Abstract
Enterohaematotrema Mehra, 1940 is emended herein based upon a review of the literature and a description of a new species (Enterohaematotrema triettruongi n. sp.) infecting yellow-headed temple turtles, Heosemys annandalii (Boulenger) (Cryptodira: Geoemydidae), in the Mekong River, Vietnam. The new species differs from the published descriptions of its congeners Enterohaematotrema palaeorticum Mehra, 1940 and Enterohaematotrema hepaticum (Simha, 1958) Simha & Chattopadhyaya, 1980 by having two distinctive oesophageal glands, a short and eversible cirrus (vs protrusive with 3 distinct processes), a dorsal common genital pore that is sinistral (vs ventral and medial), a transverse (vs longitudinal) external seminal vesicle, an oviducal seminal receptacle that is sinistral (vs dextral), and a vitellarium distributing from the caecal bifurcation (anterior to the ventral sucker) to the caecal tips (vs vitellarium not extending anteriad beyond ventral sucker in E. palaeorticum or vitellarium wholly posterior to the terminal genitalia in E. hepaticum). A phylogenetic analysis of the D1-D3 domains of the nuclear large subunit ribosomal DNA (28S) recovered Enterohaematotrema and Platt Roberts & Bullard, 2016 as sister taxa that share a recent common ancestor with the clade comprising Ruavermis Dutton & Bullard, 2020 and Coeuritrema Mehra, 1933. These flukes collectively comprise a monophyletic group of southeast Asian turtle blood flukes. This analysis also indicated that the massive, longitudinal metraterm of species of Enterohaematotrema and Uterotrema Platt & Pichelin, 1994 represents homoplasy (convergent evolution). The present study comprises the first morphological study of original specimens of any species of Enterohematotrema in more than 50 years and is the first molecular phylogenetic placement of the genus among the various turtle blood fluke lineages.
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References
Bullard, S. A., Roberts, J. R., Warren, M. B., Dutton, H. R., Whelan, N. V., Ruiz, C. F., et al. (2019). Neotropical turtle blood flukes: Two new genera and species from the Amazon Basin with a key to genera and comments on marine derived lineages in South America. Journal of Parasitology,105, 497–523.
Cribb, T. H., Crespo-Picazo, J. L., Cutmore, S. C., Stacy, B. A., Chapman, P. A., & García-Párraga, D. (2017). Elucidation of the first definitively identified life cycle for a marine turtle blood fluke (Trematoda: Spirorchiidae) enables informed control. International Journal for Parasitology,47, 61–67.
Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: More models, new heuristics, and parallel computing. Nature Methods,9, 772.
de Buron, I., Colon, B. L., Siegel, S. V., Oberstaller, J., Rivero, A., & Kyle, D. E. (2018). First evidence of polychaete intermediate hosts for Neospirorchis spp. marine turtle blood flukes (Trematoda: Spirorchiidae). International Journal for Parasitology,48, 1097–1106.
Dutton, H. R., & Bullard, S. A. (2020). Ruavermis mikebargeri gen. et sp. n. (Digenea: Schistosomatoidea) infecting the yellow-headed temple turtle, Heosemys annandalii (Cryptodira: Geoemydidae), in Vietnam, including an updated phylogeny for the turtle blood flukes. Folia Parasitologica, 67, 013.
Dutton, H. R., Warren, M. B., & Bullard, S. A. (2019). New genus and species of turtle blood fluke (Platyhelminthes: Digenea: Schistosomatoidea) infecting six-tubercled Amazon River turtles, Podocnemis sextuberculata (Pleurodira: Podocnemididae) from the Amazon River Basin (Peru). Journal of Parasitology,105, 671–685.
Glez-Peña, D., Gómez-Blanco, D., Reboiro-Jato, M., Fdez-Riverola, F., & Posada, D. (2010). ALTER: program-oriented format conversion of DNA and protein alignments. Nucleic Acids Research. Web Server issue. ISSN: 0305-1048. http://dx.doi.org/10.1093/nar/gkq321.
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.
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., et al. (2012). Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics,28, 1647–1649.
Mehra, H. R. (1940). A new distome Enterohaematotrema ng and a new blood fluke Hemiorchis bengalensis n. sp. belonging to the family Spirorchidae Stunkard, and a new species of the genus Dendritobilharzia Skrjabin and Zakharow belonging to the family Schistosomatidae Poche, with remarks on the evolution of the blood flukes. Proceedings of the National Academy of Sciences, India. Section B., 10, 100−118.
Orélis-Ribeiro, R., Halanych, K. M., Dang, B. T., Bakenhaster, M. D., Arias, C. R., & Bullard, S. A. (2017). Two new species of Elopicola (Digenea: Aporocotylidae) from Hawaiian ladyfish, Elops hawaiensis (Eastern Sea) and Atlantic tarpon, Megalops atlanticus (Gulf of Mexico) with a comment on monophyly of elopomorph blood flukes. Parasitology International,66, 305–318.
Pereira, A. G., Sterli, J., Moreira, F. R. R., & Schrago, C. G. (2017). Multilocus phylogeny and statistical biogeography clarify the evolutionary history of major lineages of turtles. Molecular Phylogenetics and Evolution,113, 59–66.
Platt, T. R. (1992). A phylogenetic and biogeographic analysis of the genera of Spirorchinae (Digenea: Spirorchidae) parasitic in freshwater turtles. Journal of Parasitology,78, 616–629.
Platt, T. R., & Blair, D. (1996). Two new species of Uterotrema (Digenea: Spirorchidae) parasitic in Emydura kreffti (Testudines: Chelidae) from Australia. Journal of Parasitology,82, 307–311.
Platt, T. R., & Pichelin, S. (1994). Uterotrema australispinosa n. gen., n. sp. (Digenea: Spirorchidae), a parasite of a freshwater turtle Emydura macquarii from southern Queensland, Australia. Journal of Parasitology,80, 1008–1011.
Rambaut, A., Suchard, M. A., Xie, D., & Drummond, A. J. (2014). FigTree v1.4.3. http://tree.bio.ed.ac.uk/software/figtree. Accessed 25 Nov 2018.
Rhodin, A. G. J., Iverson, J. B., Bour, R., Fritz, U., Georges, A., Shaffer, H. B., & van Dijk, P. P. (Turtle Taxonomy Working Group). (2017). Turtles of the world: Annotated checklist and atlas of taxonomy, synonymy, distribution, and conservation status, 8th ed. Chelonian Research Monographs 7. Lunenburg, Massachusetts: Chelonian Research Foundation and Turtle Conservancy, 292 pp.
Roberts, J. R., & Bullard, S. A. (2017). Revision and new species of Vasotrema Stunkard, 1926 (Digenea: Schistosomatoidea): turtle blood flukes of North American softshell turtles (Testudines: Trionychidae: Apalone spp.). Journal of Parasitology,103, 519–540.
Roberts, J. R., Arias, C. R., Halanych, K. M., Dang, B. T., & Bullard, S. A. (2018a). A new genus and species of turtle blood fluke (Digenea: Schistosomatoidea) from the Mekong snail-eating turtle, Malayemys subtrijuga (Schlegel & Müeller) (Testudines: Geomydidae) in Vietnam, with a reassessment of related Asiatic turtle blood flukes and molecular phylogeny. Systematic Parasitology,95, 133–145.
Roberts, J. R., Halanych, K. M., Arias, C. R., Curran, S. S., & Bullard, S. A. (2018b). A new species of Spirorchis MacCallum, 1918 (Digenea: Schistosomatoidea) and Spirorchis scripta Stunkard, 1923 infecting river cooter, Pseudemys concinna (Le Conte, 1830), (Testudines: Emydidae) in the Pascagoula River, Mississippi, U.S.A., including an updated phylogeny for Spirorchis spp. Comparative Parasitology,85, 120–132.
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., Platt, T. R., Orélis-Ribeiro, R., & Bullard, S. A. (2016a). New genus of blood fluke (Digenea: Schistosomatoidea) from Malaysian freshwater turtles (Geoemydidae) and its phylogenetic position within Schistosomatoidea. Journal of Parasitology,102, 451–462.
Roberts, J. R., Orélis-Ribeiro, R., Dang, B. T., Halanych, K. M., & Bullard, S. A. (2016b). 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, Vietnam. Folia Parasitologica,63, 031.
Roberts, J. R., Orélis-Ribeiro, R., Halanych, K. M., Arias, C. R., & Bullard, S. A. (2016c). 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., Warren, M. B., Halanych, K. M., & Bullard, S. A. (2019). Spirorchis spp. (Digenea: Schistosomatoidea) infecting map turtles (Cryptodira: Emydidae: Graptemys spp.) in southeastern North America: A new species, molecular phylogenies, and key to species. Systematic Parasitology,96, 51–64.
Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics,19, 1572–1574.
Shrivastava, P. S. (1959). Cercaria of Enterohaematotrema palaeorticum Mehra, 1940. Proceedings of the First All Indian Science Congress Association in Zoology,2, 460–465.
Simha, S. S. (1958). Studies on the trematode parasites of reptiles found in Hyderabad State. Zeitschrift für Parasitenkunde,18, 161–218.
Simha, S. S., & Chattopadhyaya, D. R. (1978). Studies on the trematode parasites of reptiles found in India. Contribution to the knowledge of blood flukes from the marine turtles, from the Gulf of Manar, South India. Journal of the Zoological Society of India,30, 69–82.
Yamaguti, S. (1971). Synopsis of digenetic trematodes of vertebrates. Tokyo: Keigaku Publishing Co., 1074 pp.
Acknowledgements
We thank Triet Nhat Truong (Aquatic Parasitology Laboratory, Auburn University, Auburn, USA) for coordinating the collection of parasites in Vietnam.
Funding
This study was supported by research grants from Auburn University’s Office of the Vice President for Research and Economic Development, the Southeastern Cooperative Fish Parasite and Disease Project (Alabama Department of Conservation and Natural Resources), and the Alabama Agriculture Experiment Station.
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All applicable institutional, national and international guidelines for the care and use of animals were followed. Sampling was approved by the Peopleʼs Committee of Dong Thap Province (permit no. 85/UBND-ĐN/ 30 August 2018).
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Dutton, H.R., Bullard, S.A. A new species and emendation of the seldom reported Enterohaematotrema Mehra, 1940 (Digenea: Schistosomatoidea), including a revised phylogenetic hypothesis for turtle blood flukes. Syst Parasitol 97, 335–345 (2020). https://doi.org/10.1007/s11230-020-09920-w
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DOI: https://doi.org/10.1007/s11230-020-09920-w