Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 5403 No. 1: 18 Jan. 2024
Type: Article
Published: 2024-01-18
DOI: 10.11646/zootaxa.5403.1.9
Page range: 130-140
Abstract views: 174
PDF downloaded: 16

A reevaluation and redescription of the branchiobdellidan Sathodrilus tetrodonta (Pierantoni, 1906) new comb. (Annelida: Clitellata)

Department of Science; University of Maine at Presque Isle; Maine 04769; USA
Annelida Branchiobdellida Branchiobdella tetrodonta Sathodrilus attenuatus taxonomy California USA ectosymbiont Pacifastacus klamathensis

Abstract

The questionable status of Branchiobdella tetrodonta Pierantoni, 1906 is resolved and the species is transferred to the correct genus. The original description was made from specimens removed from signal crayfish collected in California, USA, unfortunately, Pierantoni (1906c) did not designate any type specimens nor where the preparations were deposited; they are now presumed lost. Holt (1967) believed B. tetrodonta possessed unique penial hooks and a chitinous sheath which was due to his mistranslation of the original Italian description. As a result, Sathodrilus attenuatus Holt, 1981, was described even though specimens came from the same area and host and possessed very similar jaw characteristics to B. tetrodonta. In addition, the jaw characteristics of both endemic species are unique in the Pacific Ocean drainage of the USA. A reassessment of the literature and re-examination of Holt’s type specimens has resulted in the species name becoming a new combination, Sathodrilus tetrodonta (Pierantoni, 1906), with Sathodrilus attenuatus Holt, 1981, as its junior synonym.

 

References

  1. Bănărescu, P. (1990) Zoogeography of Fresh Waters. Aula-Verlag, Wiesbaden, 1617 pp.
  2. Bely, A.E. (2006) Distribution of segment regeneration ability in the Annelida. Integrative and Comparative Biology, 46, 508–518. https://doi.org/10.1093/icb/icj051
  3. Brinkhurst, R.O. & Gelder, S.R. (2001) Annelida: Oligochaeta and Branchiobdellida. In: Thorpe, J.H. & Covich, F. (Eds.), Ecology and Classification of North American Freshwater Invertebrates. Academic Press, New York, New York, pp. 431–463. https://doi.org/10.1016/B978-012690647-9/50013-2
  4. Brown, B.L., Turnbull, M., Skelton, J. & Creed, R.P. (2016) Ectosymbiotic cleaners induce down-regulation of crayfish immune response genes. Freshwater Crayfish, 22, 43–51. https://doi.org/10.5869/fc.2016.v22-1.43
  5. Brown, R.W. (1956) Composition of scientific words. Smithsonian Books, Washington, D.C., pp. 882.
  6. Crandall, K.A. & De Grave, S. (2017) An updated classification of the freshwater crayfishes (Decapoda: Astacidea) of the world, with a complete species list. Journal of Crustacean Biology, 37, 615–653. https://doi.org/10.1093/jcbiol/rux070
  7. Dana, J.D. (1852) United States Exploring Expedition during the years 1838, 1839, 1840, 1841, 1842, under the Command of Charles Wilkes, U.S.N. Vol. 13. Crustacea. Part I. C. Sherman, Philadelphia, 96 pls. (atlas, 1855).
  8. Ellis, M.M. (1912) A new discodrilid worm from Colorado. Proceedings of the United States National Museum, 42, 481–486. https://doi.org/10.5479/si.00963801.42-1912.481
  9. Ellis, M.M. (1919) The branchiobdellid worms in the collections of the United States National Museum, with descriptions of new genera and new species. Proceedings of the United States National Museum, 55, 241–265.
  10. https://doi.org/10.5479/si.00963801.55-2267.241
  11. Farrell, K.J., Creed, R.P. & Brown, B.L. (2014) Reduced densities of ectosymbiotic worms (Annelida: Branchiobdellida) on reproducing female crayfish. Southeastern Naturalist, 13, 523–529. https://doi.org/10.1656/058.013.0312
  12. Gelder, S.R. (1996) A review of the taxonomic nomenclature and a checklist of the species of the Branchiobdellae (Annelida: Clitellata). Proceedings of the Biological Society of Washington, 109, 653–663.
  13. Gelder, S.R. (2005) First Report of Branchiobdellidans from Lake Tahoe. Crayfish Newsletter, 27, 156–157.
  14. Gelder, S.R. (2016) Subclass Branchiobdellidea. In: Thorp, J., Rogers, D.C. (Eds.), Keys to Nearctic Fauna: Thorp and Covich’s Freshwater Invertebrates. Vol. II. Academic Press, New York, New York, pp. 234–244. https://doi.org/10.1016/B978-0-12385028-7.00012-3
  15. Gelder, S.R. (2019) Subclass Branchiobdellida. In: Thorp, J., Rogers, D.C. (Eds.), Keys to Palaearctic Fauna: Thorp and Covich’s Freshwater Invertebrates. Vol. 4. Academic Press, New York, New York, pp. 483–491.
  16. Gelder, S.R. (2020). An ongoing saga: Endemic branchiobdellidans (Annelida: Clitellata) on translocated commercial North American crayfish. Zoosymposia, 17, 141–158. https://doi.org/10.11646/zoosymposia.17.1.13
  17. Gelder, S.R., Gagnon, N.L. & Nelson, K. (2002) Taxonomic considerations and distribution of the Branchiobdellida (Annelida: Clitellata) on the North American continent. Northeastern Naturalist, 9, 451–468. https://doi.org/10.1656/1092-6194(2002)009[0451:TCADOT]2.0.CO;2
  18. Gelder, S.R. & Hall, L.A. (1990) Description of Xironogiton victoriensis n.sp. from British Columbia, Canada, with remarks on other species and a Wagner analysis of Xironogiton (Clitellata: Branchiobdellida). Canadian Journal of Zoology, 68, 2352–2359. https://doi.org/10.1139/z90-326
  19. Gelder, S.R., Parpet, J.-F. & Ohtaka, A. (2020) Early researchers involved with branchiobdellidans (Annelida: Clitellata) on Japanese crayfish, and a reassessment of the taxonomic status of Branchiobdella digitata Pierantoni, 1906. Acta Zoologica Bulgarica, 72, 179–185.
  20. Gelder, S.R. Parpet, J.-F. & Quaglio, F. (2012) First report of two North American branchiobdellidans (Annelida: Clitellata) or crayfish worms on Signal crayfish in Europe with a discussion of similar introductions into Japan. Annales de Limnologie—International Journal of Limnology, 48, 315–322. https://doi.org/10.1051/limn/2012021
  21. Gelder, S.R. & Siddall, M.E. (2001) Phylogenetic assessment of the Branchiobdellidae (Annelida, Clitellata) using 18S rDNA, mitochondrial cytochrome c oxidase subunit I and morphological characters. Zoologica Scripta, 30, 215–222. https://doi.org/10.1046/j.1463-6409.2001.00063.x
  22. Gelder, S.R. & Williams, B.W. (2011) First distributional study of Branchiobdellida (Annelida: Clitellata) in the Great Smoky Mountain National Park, North Carolina and Tennessee, USA, with a redescription of Cambarincola holostomus Hoffman, 1963. Southeastern Naturalist, 10, 211–220. https://doi.org/10.1656/058.010.0202
  23. Gelder, S.R. & Williams, B.W. (2015) Clitellata: Branchiobdellida. In: Thorp, J. & Rogers, D.C. (Eds.), Thorp and Covich’s Freshwater Invertebrates: Ecology and Biology. Vol. I. Academic Press, New York, New York, pp. 551–563. https://doi.org/10.1016/B978-0-12-385026-3.00022-X
  24. Gelder, S.R. & Williams, B.W. (2016) Global Overview of Branchiobdellida (Annelida: Clitellata). In: Kawai, T., Faulkes, Z. & Scholtz, G. (Eds.), Freshwater Crayfish: A Global Overview. CRC Press, New York, New York, pp. 628–654. https://doi.org/10.1201/b18723-27
  25. Goodnight, C.J. (1939) Geographical distribution of North American branchiobdellids. Journal of Parasitology, 25, 11.
  26. Goodnight, C.J. (1940a) The Branchiobdellidae (Oligochaeta) of North American crayfish. Illinois Biological Monographs, 17, 1–75. https://doi.org/10.5962/bhl.title.50176
  27. Goodnight, C.J. (1940b) New records of branchiobdellids (Oligochaeta) and their crayfish hosts. Report of the Reelfoot Lake Biological Station, 4, 170–171.
  28. Hall, M.C. (1914) Descriptions of a new genus and species of the discodrilid worms. Proceedings of the United States National Museum, 48, 187–193. https://doi.org/10.5479/si.00963801.48-2071.187
  29. Hoffman, R.L. (1963) A revision of the North American annelid worms of the genus Cambarincola (Oligochaeta: Branchiobdellidae). Proceedings of the United States national Museum, 114, 271–371. https://doi.org/10.5479/si.00963801.114-3470.271
  30. Holt, P.C. (1967) Status of genera Branchiobdella and Stephanodrilus in North America with description of a new genus (Clitellata: Branchiobdellida). Proceedings of the United States National Museum, 124, 1–10. https://doi.org/10.5479/si.00963801.124-3631.1
  31. Holt, P.C. (1968b) New genera and species of branchiobdellid worms (Annelida: Clitellata). Proceedings of the Biological Society of Washington, 81, 291–318.
  32. Holt, P.C. (1981) New species of Sathodrilus Holt, 1968, (Clitellata: Branchiobdellida) from the Pacific drainage of the United States, with the synonymy of Sathodrilus virgiliae Holt, 1977. Proceedings of the Biological Society of Washington, 94, 848–862.
  33. Hoshino, T., Ohtaka, A. & Smith, R.J. (2023) New records of the signal crayfish and its ectosymbiotic branchiobdellidan and ostracod from Lake Sugenuma in Gunma Prefecture, central Japan. Bulletin of Gunma Museum of Natural History, 27, 99–106. [in Japanese with English abstract]
  34. ICZN International Commission on Zoological Nomenclature (1999). Available from: http://www.nhm.ac.uk/hosted-sites/iczn/code/ (accessed 15 February 2023) https://doi.org/10.5479/si.00963801.124-3631.1
  35. Kawai, T. Mitamura, T. & Ohtaka, A. (2004) The taxonomic status of the introduced North American signal crayfish, Pacifastacus leniusculus (Dana, 1852) in Japan, and the source of specimens in the newly reported population in Fukushima Prefecture. Crustaceana, 77, 861–870. https://doi.org/10.1163/156854004774248735
  36. Kaygorodova, I.A. & Sherbakov, D.Yu. (2006) Molecular Phylogenetic Study of the Systematic Position of BaikalianOligochaetes in Clitellata. Russian Journal of Genetics, 42, 1390–1397. https://doi.org/10.1134/S1022795406120052
  37. Kim, C.B., Moon, S.Y. Gelder, S.R. & Kim, W. (1996) Phylogenetic Relationships of Annelids, Molluscs, and Arthropods Evidenced from Molecules and Morphology. Journal of molecular evolution, 43, 207–215. https://doi.org/10.1007/BF02338828
  38. Kitano, S., Ishizuka, T., Murakami, M., Sawamoto, Y., Ushio, N. & Ohtaka, A. (2022) New records of nonnative signal crayfish (Pacifastacus leniusculus) in Nagano Prefecture with implications for multiple translocation pathways. Japanese Journal of Conservation Ecology, 27, 43–53. [in Japanese with English abstract] https://doi.org/10.18960/hozen.2126
  39. Kobayashi, Y. (2012) Symposium on alien crayfish—Focusing on the specified alien species specified by the Ministry of Environment, Crayfish. Cancer, 21, 93–94. https://doi.org/10.18988/cancer.21.0_93
  40. Larson, E.R. & Williams, B.W. (2016) Historical biogeography of Pacifastacus crayfishes and their branchiobdellian and entocytherid ectosymbionts in western North America. In: Kawai, T., Faulkes, Z. & Scholtz, G. (Eds.), Freshwater Crayfish: A Global Overview. CRC Press, Boca Raton, Florida, pp. 404–447. https://doi.org/10.1201/b18723-21
  41. Leidy, J. (1851) Contributions to Helminthology. Proceedings of the Academy of Natural Sciences of Philadelphia, 5, 205–209.
  42. Longshaw, M. (2016) Parasites, Commensals, Pathogens and Diseases of Crayfish. In: Longshaw, M. & Stebbings, P. (Eds.), Biology and Ecology of crayfish. CRC Press, Boca Raton, Florida, 669 pp. https://doi.org/10.1201/b20073
  43. Martin, P. (2001) On the origin of the Hirudinea and the demise of the Oligochaeta. Proceedings of the Royal Society of London, B268, 1089–1098. https://doi.org/10.1098/rspb.2001.1616
  44. Martin, P., Kaygorodova, I., Sherbakov, D.Y. & Verheyen, E. (2000) Rapidly evolving lineages impede the resolution of phylogenetic relationships among Clitellata (Annelida). Molecular Phylogenetics and Evolution, 15, 355–368. https://doi.org/10.1006/mpev.1999.0764
  45. Nakata, K., Hayashi, N., Ozaki, M., Ohtaka, A. & Miwa, J. (2010) First record of the North American invasive crayfish Pacifastacus leniusculus from the Kanto region, Tone River basin, central Japan: a range expansion to a warm water area. Plankton & Benthic Research, 5, 165–168. https://doi.org/10.3800/pbr.5.165
  46. Ohtaka, A. (2007) Distribution of exotic branchiobdellidans (Annelida: Clitellata) in Japan. Japanese Journal of Limnology, 68, 483–489. https://doi.org/10.3739/rikusui.68.483
  47. Ohtaka, A. (2010) Community Conservation. In: Kawai, T. & Takahata, M. (Eds.), Biology of Crayfish. Hokkaido Daigaku Shuppankai, Sapporo, pp. 445–475. [in Japanese]
  48. Ohtaka, A. & Gelder, S.R. (2023) A taxonomic reassessment of Cirrodrilus japonicus (Pierantoni, 1912) (Annelida, Clitellata, Branchiobdellida). Zootaxa, 5263 (4), 557–565. https://doi.org/10.11646/zootaxa.5263.4.7
  49. Ohtaka, A., Gelder, S.R., Kawai, T., Saito, K., Nakata, K. & Nishino, M. (2005) New records and distribution of two North American branchiobdellidan species (Annelida: Clitellata) from introduced Signal Crayfish, Pacifastacus leniusculus, in Japan. Biological Invasion, 7, 149–156. https://doi.org/10.1007/s10530-004-8146-y
  50. Pierantoni, U. (1905) Cirrodrilus cirratus n.g. n. sp. parassita dell’ Astacus japonicus. Annuario del Museo Zoologico della R. Università di Napoli, 1, 1–3.
  51. Pierantoni, U. (1906a) Osservazioni sul Branchiobdella Odier. Annuario Museo zoologico della Rigia Università di Napoli, 2, 1–10.
  52. Pierantoni, U. (1906b) Osservazioni sul genere Branchiobdella Odier. Rivista mensile di pesca e idrobioloia, 8, 1–11.
  53. Pierantoni, U. (1906c) Nuovi Discodrilidi del Giappone e della California. Annuario Rigia Museo zoologico della R. Università di Napoli, 2, 1–9.
  54. Pierantoni, U. (1912) Monografia dei Discodrilidae. Annuario del Museo Zoologico della Rigia Università di Napoli, New Series, 3, 1–27.
  55. Rebel, H. (1938) Reisebriefe Franz Steindachners aus Amerika. s.n., Wein, 65pp.
  56. Robinson, D.A. (1954) Cambarincola gracilis sp. nov., a branchiobdellid oligochaete commensal on western crayfishes. Journal of Parasitology, 40, 466–469. https://doi.org/10.2307/3273899
  57. Rousset, V., Plaisance, L., Erséus, C., Siddall, M.E. & Rouse, G.W. (2008) Evolution of habitat preference in Clitellata (Annelida). Biological Journal of the Linnean Society, 95, 447–464. https://doi.org/10.1111/j.1095-8312.2008.01072.x
  58. Shida, Y. & Kawai, T. (2022) Species identification of recently established alien freshwater crayfish in Niigata Prefecture, Japan, with implication of their origin based on ectosymbiotic branchiobdellidan composition. Izunuma-Uchinuma Wetland Researches, 16, 21–32. [in Japanese with English abstract]
  59. Siddall, M.E., Apakupakul, K., Burreson, E.M., Coates, K.A., Erséus, C., Gelder, S.R., Källersjö, M. & Trapido-Rosenthal, H. (2001) Validating Livanow: Molecular Data Agree that Leeches, Branchiobdellidans, and Acanthobdella peledina form a Monophyletic Group of Oligochaetes. Molecular Phylogenetics and Evolution, 21, 346–351. https://doi.org/10.1006/mpev.2001.1021
  60. Stimpson, W. (1857) Notices of new species of Crustacea of western North America; being an abstract from a paper to be published in the journal of the society. Proceedings of the Boston Society of Natural History, 6, 84–89. https://doi.org/10.5962/bhl.part.15468
  61. Subchev, M.A. (2014) Genus Branchiobdella Odier, 1823: A review of its European species. Acta zoologica Bulgarica, 66, 5–20.
  62. Subchev, M.A. & Gelder, S.R. (2010) Branchiobdellida (Annelida: Clitellata) found in the crayfish collection of the Natural History Museum of Vienna, Austria, with a redescription of Branchiobdella papillosa Nesemann & Hutter, 2002. Acta zoologica Bulgarica, 62, 33–42.
  63. Tessler, M., de Carle, D., Voiklis, M.L., Gresham, O.A., Neumann, J.S., Cios, S. & Siddall, M.E. (2018) Worms that suck: Phylogenetic analysis of Hirudinea solidifies the position of Acanthobdellida and necessitates the dissolution of Rhynchobdellida. Molecular Phylogenetics and Evolution, 127, 129–134. https://doi.org/10.1016/j.ympev.2018.05.001
  64. Timm, T. (1991) Branchiobdellida (Oligochaeta) from the farthest South-East of the U.S.S.R. Zoologica Scripta, 20, 321–331.
  65. https://doi.org/10.1111/j.1463-6409.1991.tb00297.x
  66. Timm, T. (1999) Distribution of freshwater oligochaetes in the west and east coastal regions of the North Pacific Ocean. Hydrobiologia, 406, 67–81. https://doi.org/10.1023/A:1003749519662
  67. Vedia, I., Miranda, R., Oscoz, J. & Baquero, E. (2016) Invading the invaders: relationships of an exotic branchiobdellidan with its exotic host and environmental conditions. Inland Waters, 6, 54–64. https://doi.org/10.5268/IW-6.1.895
  68. Williams, B.W., Gelder, S.R., Proctor, H. & Coltman, D.W. (2013) Molecular phylogeny of North American Branchiobdellida (Annelida: Clitellata). Molecular Phylogenetics and Evolution, 66, 30–42. https://doi.org/10.1016/j.ympev.2012.09.002
  69. Williams, B.W. & Weaver, P.G. (2021) Asymmetrical host switching by two groups of obligate ectosymbionts of crayfishes. Western North American Naturalist, 81, 63–70. https://doi.org/10.3398/064.081.0106
  70. Winnepenninckx, B.M.H., Van de Peer, Y. & Backeljau, T. (1998) Metazoan Relationships on the Basis of 18S rRNA Sequences: A Few Years Later. American Zoologist, 38, 888–906. https://doi.org/10.1093/icb/38.6.888
  71. Yamaguchi, H. (1934) Studies on Japanese Branchiobdellidae with some revisions on the classification. Journal of the Faculty of Science, Hokkaido University, Series VI, Zoology, 3, 177–219.
  72. Yamauchi, Y. & Kawai, T. (2022) Salinity tolerance of the alien branchiobdellidan Sathodrilus attenuatus (Annelida: Clitellata)on the introduced freshwater crayfish Pacifastacus leniusculus (Crustacea: Decapoda) in eastern Hokkaido, Japan and the pathway of introduction of the host to Lake Harutori and adjacent freshwaters in Kushiro City, eastern Hokkaido. Wetland Researches, 16, 47–62.