Folia Parasitologica, vol. 63 (2016)

Folia Parasitologica 63:041 (2016) | DOI: 10.14411/fp.2016.041

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

Jackson R. Roberts1, Raphael Orélis-Ribeiro2, Kenneth M. Halanych3, Cova R. Arias4, Stephen A. Bullard1
1 Aquatic Parasitology Laboratory, School of Fisheries, Aquaculture, and Aquatic Sciences, Auburn University, Auburn, Alabama, USA;
2 Laboratório de Ecologia Molecular e Parasitologia Evolutiva, Universidade Federal do Paraná, Curitiba, Paraná, Brazil;
3 Auburn University, Department of Biological Sciences and Molette Biology Laboratory for Environmental & Climate Change Studies, Auburn, Alabama, USA
4 Aquatic Microbiology Laboratory, School of Fisheries, Aquaculture, and Aquatic Sciences, Auburn University, Auburn, Alabama, USA

Chicken turtles, Deirochelys reticularia (Latreille in Sonnini et Latreille) (Testudines: Emydidae) from Alabama, USA were infected by Spirorchis collinsi Roberts et Bullard sp. n. and Spirorchis cf. scripta. The new species is most easily differentiated from its congeners by the combination of having caeca that extend far beyond the genitalia, intercaecal genitalia positioned in the middle portion of the body, a testicular column that nearly abuts the caecal bifurcation, a cirrus sac positioned between the testes and ovary, a massive Mehlis' gland, an elongate, longitudinal metraterm that extends anteriad beyond the level of the ovary, a pre-ovarian genital pore, and a prominent, intercaecal Manter's organ. The specimens of S. cf. scripta differed from the holotype and published descriptions of Spirorchis scripta Stunkard, 1923 by several subtle morphological features, perhaps comprising intraspecific variation, but collectively warranted a detailed description herein. Based on examinations of the aforementioned specimens plus the holotype, paratypes and vouchers of morphologically-similar congeners, Spirorchis MacCallum, 1918 is emended to include the presence of oral sucker spines, a pharynx, lateral oesophageal diverticula ('plicate organ') and a median oesophageal diverticulum ('oeseophageal pouch'). Phylogenetic analysis of the nuclear large subunit rDNA (28S) recovered S. collinsi sister to Spirorchis picta Stunkard, 1923, > 99% similarity between S. cf. scripta and S. scripta, and a monophyletic Spirorchis MacCallum, 1918. No blood fluke infection has been reported previously from these drainages, Alabama, or this turtle species. This is the first new species of Spirorchis to be described from North America in 26 years.

Received: September 10, 2016; Accepted: October 26, 2016; Published online: December 20, 2016


References

  1. Anonymous. 1919: Twenty-third Annual Report of the New York Zoological Society. Clark and Fritts Printers, New York, 204 pp.
  2. Bodie J.R., Semlitsch R.D. 2000: Spatial and temporal use of floodplain habitats by lentic and lotic species of aquatic turtles. Oecologia 122: 138-146. Go to original source... Go to PubMed...
  3. Brooks D.R., Palmieri J.R. 1979: Neopronocephalus orientalis sp. n. (Digenea: Pronocephalidae) and Spirhapalum elongatum Rohde, Lee, and Lim, 1968 (Digenea: Spirorchiidae) from Cuora amboinensis (Daudin) in Malaysia. Proc. Helminthol. Soc. Wash. 46: 55-57. Go to PubMed...
  4. Buhlmann K.A. 2005: Habitat use, terrestrial movements, and conservation of the turtle, Deirochelys reticularia in Virginia. J. Herpetol. 29: 173-181. Go to original source...
  5. Bullard S.A. 2012: A new aporocotylid (Digenea) species from blood vascular system of gag grouper, Mycteroperca microlepis (Perciformes: Serranidae), off Alabama, with an emendation of Pearsonellum Overstreet & Køie, 1989. J. Parasitol. 98: 323-327. Go to original source... Go to PubMed...
  6. Bullard S.A. 2013: Cardicola langeli n. sp. (Digenea: Aporocotylidae) from heart of sheepshead, Archosargus probatocephalus, (Actinopterygii: Sparidae) in the Gulf of Mexico, with an updated list of hosts, infection sites and localities for Cardicola spp. Folia Parasitol. 60: 17-27. Go to original source... Go to PubMed...
  7. Bullard S.A, Snyder S.D., Jensen K., Overstreet R.M. 2008: New genus and species of Aporocotylidae (Digenea) from a lower actinopterygian, the American paddlefish, Polyodon spathula, (Polyodontidae) from the Mississippi Delta. J. Parasitol. 94: 487-495. Go to original source... Go to PubMed...
  8. Byrd E.E. 1939: Studies on the blood flukes of the family Spirorchidae. Part II. Revision of the family and description of new species. J. Tenn. Acad. Sci. 14: 116-161.
  9. van Dijk P.P., Iverson J.B., Rhodin A.G. J., Shaffer H.B., Bour R. 2014: Turtles of the world. Seventh Edition. Annotated checklist of taxonomy, synonymy, distribution with maps, and conservation status. Chel. Res. Monogr. 5: 329-479. Go to original source...
  10. Ejsmont L. 1927: Spirhapalum polesianum n. g., n. sp. trématode du sang d'Emys orbicularis L. Ann. Parasitol. Hum. Comp. 5: 220-235.
  11. Ernst C.H., Lovich J.E. 2009: Turtles of the United States and Canada. Second Edition. The Johns Hopkins University Press, Baltimore, Maryland, 827 pp.
  12. Goodchild C.G., Kirk D.E. 1960: The life history of Spirorchis elegans Stunkard, 1923 (Trematoda: Spirorchiidae) from the painted turtle. J. Parasitol. 46: 219-229. Go to original source... Go to PubMed...
  13. Goodchild C.G., Martin V.L. 1969: Speciation in Spirorchis (Trematoda: Spirorchiidae) infecting the painted turtle, Chrysemys picta. J. Parasitol. 55: 1169-1173. Go to original source...
  14. Guillon J., Guéry L., Hulin V., Girondot M. 2012: A large phylogeny of turtles (Testudines) using molecular data. Contr. Zool. 81: 147-158.
  15. Gupta N.K., Mehrotra V. 1975: On three blood flukes (Spirorchiidae: Spirorchiinae) from freshwater chelonians and discussion on the synonymy of Plasmiorchis pellucidus Mehra, 1934. Riv. Parassitol. 36: 165-170.
  16. Guyer C., Bailey M.A., Mount R.H. 2015: Turtles of Alabama, The University of Alabama Press, Tuscaloosa, Alabama, 266 pp.
  17. Holliman R.B., Fisher J.E. 1968: Life cycle and pathology of Spirorchis scripta Stunkard, 1923 (Digenea: Spirochiidae) in Chrysemys picta picta. J. Parasitol. 54: 310-318. Go to original source... Go to PubMed...
  18. Holliman R.B., Fisher J.E., Parker J.C. 1971: Studies on Spirorchis parvus (Stunkard, 1923) and its pathological effects on Chrysemys picta picta. J. Parasitol. 57: 71-77. Go to original source... Go to PubMed...
  19. Johnson P.D., Bogan A.E., Brown K.M., Burkhead N.M., Cordeiro J.R., Garner J.T., Hartfield P.D., Lepitzki D.A.W., Mackie G.L., Pip E., Tarpley T.A., Tiemann J.S., Whelan N.V., Strong E.E. 2013: Conservation status of freshwater gastropods of Canada and the United States. Fisheries. 38: 247-282. Go to original source...
  20. Lockyer A.E., Olson P.D., Ostergaard P., Rollinson D., Johnston D.A., Attwood S.W., Southgate V.R., Horák P., Snyder S.D., Le T.H., Agatsuma T., McManus D.P., Carmichael A.C., Naem S., Littlewood D.T.J. 2003: The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126: 203-224. Go to original source... Go to PubMed...
  21. MacCallum G.A. 1918: Notes on the genus Telorchis and other trematodes. Zoopathologica 1: 77-98.
  22. MacCallum G.A. 1926: Revue du genre Spirorchis MacCallum. Ann. Parasitol. Hum. Comp. 4: 97-103.
  23. McVay M.J., Bakenhaster M.D., Bullard S.A. 2011: Cardicola laruei Short, 1953 (Digenea: Aporocotylidae) from heart of seatrouts, Cynoscion spp., (Perciformes: Sciaenidae) in the Gulf of Mexico and Atlantic Ocean: taxonomic redescription, first observations of egg and miracidium, and comments on geographic distribution and host specificity. Comp. Parasitol. 78: 291-305. Go to original source...
  24. Mehra H.R. 1934: 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 II. Bull. Acad. Sci. United Prov. Agra Oudh 3: 169-196.
  25. Mehra H.R. 1939: New blood flukes of the family Spirorchidae Stunkard (Trematoda) from the marine turtle Chelone mydas of the Arabian Sea with observations on the synonymity of certain genera and classification of the family. Proc. Nat. Acad. Sci. India 9: 155-167.
  26. Olson P.D., Cribb T.H., Tkach V.V., Bray R.A., Littlewood D.T.J. 2003. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int. J. Parasitol. 33: 733-755. Go to original source... Go to PubMed...
  27. Orélis-Ribeiro R., Arias C.R., Halanych K.M., Cribb T.H., Bullard S.A. 2014: Diversity and ancestry of flatworms infecting blood of nontetrapod craniates "fishes." Adv. Parasitol. 85: 1-64.
  28. Pieper M.B. 1953: The life history and germ cell cycle of Spirorchis artericola (Ward, 1921). J. Parasitol. 39: 310-325. Go to original source... Go to PubMed...
  29. Platt T.R. 1990: Aphanospirorchis kirki n. gen., n. sp. (Digenea: Spirorchidae), a parasite of the midland painted turtle, Chrysemys picta marginata, from northwestern Indiana, with comments on the proper spelling of the family name. J. Parasitol. 76: 650-652. Go to original source...
  30. Platt T.R. 1992: A phylogenetic and biogeographic analysis of the genera of Spirorchinae (Digenea: Spirorchidae) parasitic in freshwater turtles. J. Parasitol. 78: 616-629. Go to original source... Go to PubMed...
  31. Platt T.R. 1993: Taxonomic revision of Spirorchis MacCallum, 1919 (Digenea: Spirorchidae). J. Parasitol. 79: 337-346. Go to original source...
  32. Platt T.R. 2002: Family Spirorchiidae Stunkard, 1921. In: D.I. Gibson, A.J. Jones and R.A. Bray (Eds.), Keys to the Trematoda, Vol. 1. CABI, Wallingford, 453-467 pp.
  33. Price E.W. 1934: New genera and species of blood flukes from a marine turtle, with a key to the genera of the family Spirorchidae. J. Wash. Acad. Sci. 24: 132-141.
  34. Rathbun G.B., Scott Jr. N.J., Murphey T.G. 2002: Terrestrial habitat use by Pacific pond turtles in a Mediterranean climate. Southwest. Nat. 47: 225-235. Go to original source...
  35. Reese D.A., Welsh H.H. 1997: Use of terrestrial habitat by western pond turtles, Clemmys marmorata: implications for management. In: Proceedings: Conservation, Restoration, and Management of Tortoises and Turtles-An International Conference. New York Turtle and Tort. Soc. New York City, New York, pp. 352-357.
  36. 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 Parasitol. 63: 031. Go to original source... Go to PubMed...
  37. 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. J. Parasitol. 102: 451-462. Go to original source... Go to PubMed...
  38. Rohde K., Lee S. K., Lim H.W. 1968: Ueber drei malayische Trematoden. Ann. Parasitol. Hum. Comp. 43: 33-43. Go to PubMed...
  39. Ryan T.J, Conner C.A., Douthitt B.A., Sterrett S.C., Salsbury C.M. 2008: Movement and habitat use of two aquatic turtles (Graptemys geographica and Trachemys scripta) in an urban landscape. Urban Ecosyst. 11: 213-225. Go to original source...
  40. Sinha B.B. 1934: A new genus of blood flukes of the family Spirorchidae, from the tortoise, Hardella thurgi (Gray). Rec. Ind. Mus. 36: 147-151.
  41. 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. Helminthol. Abstr. 66: 255-294.
  42. 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. Helminthol. Abstr. 66: 329-344.
  43. Snyder S.D. 2004. Phylogeny and paraphyly among tetrapod blood flukes (Digenea: Schistosomatidae and Spirorchiidae). Int. J. Parasitol. 34: 1385-1392. Go to original source... Go to PubMed...
  44. Spinks P.Q., Thomson R.C., McCartney-Melstad E., Shaffer H.B. 2016: Phylogeny and temporal diversification of the New World pond turtles (Emydidae). Mol. Phylogenet. Evol. 103: 85-97. Go to original source... Go to PubMed...
  45. Stunkard H.W. 1922: Two new genera of North American blood flukes. Am. Mus. Novit. 39: 1-8.
  46. Stunkard H.W. 1923: Studies on North American blood flukes. Bull. Am. Mus. Nat. Hist. 48: 165-221.
  47. Thatcher V.E. 1954: Some helminthes parasitic in Clemmys marmorata. J. Parasitol. 40: 481-482. Go to original source...
  48. Tkach V., Snyder S.D., Vaughan J.A. 2009: A new species of blood fluke (Digenea: Spirorchiidae) from the Malayan box turtle, Cuora amboinensis (Cryptodira: Geoemydidae) in Thailand. J. Parasitol. 95: 743-746. Go to original source... Go to PubMed...
  49. Truong T.N., Bullard S.A. 2013: Blood flukes (Digenea: Aporocotylidae) of walking catfishes (Siluriformes: Clariidae): new genus and species from the Mekong River (Vietnam) and a note on catfish aporocotylids. Folia Parasitol. 60: 237-247. Go to original source... Go to PubMed...
  50. Ulmer M.J. 1959: Studies on Spirorchis haematobium (Stunkard, 1922) Price, 1934 (Trematoda: Spirorchiidae) in the definitive host. Trans. Am. Microsc. Soc. 78: 81-89. Go to original source...
  51. Wall L.D. 1939: Life history of Spirorchis sp. (Trematoda: Spirorchiidae). J. Parasitol. 25: 28.
  52. Wall L.D. 1940: Life history of Spirorchis parvus (Stunkard) Trematoda: Spirorchiidae. Science 92: 362-363. Go to original source... Go to PubMed...
  53. Wall L.D. 1941a: Life history of Spirorchis elephantis (Cort, 1917), a new blood fluke from Chrysemys picta. Am. Midl. Nat. 25: 402-412. Go to original source...
  54. Wall L.D. 1941b: Spirorchis parvus (Stunkard) its life history and the development of its excretory system (Trematoda: Spirorchiidae). Trans. Am. Microsc. Soc. 60: 221-260. Go to original source...
  55. Ward H.B. 1921: A new blood fluke from turtles. J. Parasitol. 114-128.