Abstract
The description of Helobdella stagnalis (Linnaeus, 1758) has emphasized the presence of a nuchal, chitinous scute located on the dorsal surface in the first third of the body as the diagnostic character for the species. Historically, identifications of species of Helobdella have relied heavily on this character and, as a result, Helobdella stagnalis has been reported from an inordinately broad geographic range, including Europe, Asia, Africa, North America, and South America. In addition to a few earlier investigations, a recent analysis showed that great genetic distances (orders of magnitude greater than previous estimations of intraspecific divergence in leeches) are present between scute-bearing specimens identified as H. stagnalis from Europe and North America, implying that H. stagnalis does not occur in North America. The present study expands the geographic boundaries of taxon sampling for both European and North American taxa, and re-examines the phylogenetic relationships and cytochrome c oxidase subunit I (COI) variation within scute-bearing species of the genus Helobdella. Our analyses include specimens putatively identified as “Helobdella stagnalis” from Sweden, Norway, Iceland, England, France, Italy, Slovenia, Turkey, Russia, and Iran, as well as numerous localities covering Canada and the USA. Our results corroborate previous studies in that European and west Asian specimens form a clade, including the neotype, which is separate from North American taxa. To alleviate future taxonomic confusion, we redescribe H. stagnalis and designate a neotype from the inferred type locality. The designation of a neotype stabilizes the taxonomy of scute-bearing leeches of the genus Helobdella and enables us to definitively correct erroneous identifications reported in previous studies. We also note that at least four lineages of scute-bearing, North American species of Helobdella lack formal descriptions.
References
Achurra, A., Rodriguez, P. & Erséus, C. (2015) Pseudo-cryptic speciation in the subterranean medium: A new species of Stylodrilus Claparède, 1862, with a revision of the status of Bichaeta Bretscher, 1900 (Annelida, Clitellata, Lumbriculidae). Zoologischer Anzeiger, 257, 71–86.
https://doi.org/10.1016/j.jcz.2015.05.003
Arslan, N. & Oktener, A. (2012) A general review of parasitic Annelida (Hirudinea) recorded from different habitats and hosts in Turkey. Turkish Journal of Zoology, 36, 141–145.
https://doi.org/10.3906/zoo-1007-15
Bayer, E. (1898) Hypodermis und neue Hautsinnesorgane der Rhynchobdelliden. Zeitschrift für wissenschaftliche Zoologie, 64, 648–696.
Bely, A.E. & Weisblat, D.A. (2006) Lessons from leeches: a call for DNA barcoding in the lab. Evolution & Development, 501, 491–501.
https://doi.org/10.1111/j.1525-142X.2006.00122.x
Beresic-Perrins, R.K., Govedich, F.R., Banister, K., Bain, B.A., Rose, D. & Shuster, S.M. (2017) Helobdella blinni sp. n. (Hirudinida, glossiphoniidae) a new species inhabiting montezuma well, Arizona, USA. ZooKeys, 2017, 137–155.
https://doi.org/10.3897/zookeys.661.9728
Bergman (1757) Afhandling om Iglar. Kungl. Svenska vetenskapsakademiens handlingar, 18, 304–314.
Blanchard, E. (1849) Annulares. In: Historia Fisica e Politica de Chile, Zoologia. En Casa Del Autor, Paris, pp. 43–50.
Blanchard, R. (1894) Hirudinées de l’Italie continentale et insulaire. Bollettino dei musei di zoologia ed anatomia comparata della R. Universit di Torino, 9, 1–84.
Blanchard, R. (1900) Hirudineen. Hamburger Magalhaensische Sammelreise, 3, 1–20.
Carena, H. (1820) Monographie du genre Hirudo. Memorie della reale Accademia delle Scienze di Torino, 25, 273–316.
de Carle, D., Oceguera-Figueroa, A., Tessler, M., Siddall, M.E. & Kvist, S. (2017) Phylogenetic analysis of Placobdella (Hirudinea: Rhynchobdellida: Glossiphoniidae) with consideration of COI variation. Molecular Phylogenetics and Evolution, 114, 234–248.
https://doi.org/10.1016/j.ympev.2017.06.017
Castle, W.E. (1900) Some North American fresh-water Rhynchobdellidae, and their parasites. Bulletin of the Museum of Comparative Zoology, 36, 18–64.
Chandra, M. & Mahajan, K. (1976) Leeches of Simla Hillsm Himachal Pradesh. Records of the Zoological Survey of India, 69, 255–259.
Cordero, E.H. (1937) Hirudíneos Neotropicales y Subantárticos Nuevos, Critícos ya conocidos del Museu Argentino de Ciencias Naturales. Anales del Museo Argentino de Ciencias Naturales, 29, 1–77.
Dalyell, J.G. (1853) 2 The Powers of the Creator displayed in the Creation: or, observations on life amidst the various forms of the humbler tribes of animated nature with practical comments and illustrations. J. Van Voorst, London, 359 pp.
Daudin, F. (1800) Description de quatre espèces de vers corps lisse. Recueil de Mémoires et de Notes, 2, 19–23.
Davies, R.W., Wrona, F.J. & Linton, L. (1979) A serological study of prey selection by Helobdella stagnalis (Hirudinoidea). Journal of Animal Ecology, 48, 181–194.
Deiner, K., Knapp, R.A., Boiano, D.M. & May, B. (2013) Increased accuracy of species lists developed for alpine lakes using morphology and cytochrome oxidase I for identification of specimens. Molecular Ecology Resources, 13, 820–831.
Derheims, J.L. (1825) Histoire Naturelle et Médicale des Sangsues. Baillière, Paris, 165 pp.
Evans, W. (1905) Additions to Scott and Lindsay’s list of animals found in the upper elf loch. The Annals of Scottish natural history, 56, 215–218.
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.
Goloboff, P.A., Farris, J.S. & Nixon, K.C. (2008) TNT, a free program for phylogenetic analysis. Cladistics, 24, 774–786.
https://doi.org/10.1111/j.1096-0031.2008.00217.x
Harding, W.A. (1930) A Revision of the British Leeches. Journal of the Linnean Society of London, Botany, 48, 467–544.
https://doi.org/10.1111/j.1095-8339.1930.tb00595.x
International Commission of Zoological Nomenclature (1999) International Code of Zoological nomemclature. 4th Edition. International Trust for Zoological Nomenclature, London, xxix + 306 pp.
Iwama, R.E. & Arruda, E.P. (2016) Leeches of the genus Helobdella (Clitellata: Hirudinida) from São Paulo, Brazil with descriptions of two new species using micro-computed tomography and a new record of Barbronia weberi (Blanchard 1897). Zootaxa, 4144 (3), 411–429.
https://doi.org/10.11646/zootaxa.4144.3.8
Johnson, R.J. (1817) Observations on the Hirudo complanata, and Hirudo stagnalis , now formed into a distinct genus under the name, Glossopora. Philosophical Transactions of the Royal Society of London, 107, 339–346.
https://doi.org/10.1098/rstl.1817.0027
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.
https://doi.org/10.1093/molbev/mst010
Kawauchi, G.Y. & Giribet, G. (2014) Sipunculus nudus Linnaeus, 1766 (Sipuncula): Cosmopolitan or a group of pseudo-cryptic species? An integrated molecular and morphological approach. Marine Ecology, 35, 478–491.
https://doi.org/10.1111/maec.12104
Kaygorodova, I.A., Mandzyak, N., Petryaeva, E. & Pronin, N.M. (2014) Genetic diversity of freshwater leeches in Lake Gusinoe (Eastern Siberia, Russia). Scientific World Journal, 2014, 1–11.
https://doi.org/10.1155/2014/619127
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649.
https://doi.org/10.1093/bioinformatics/bts199
Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular biology and evolution, 33, 1870–1874.
https://doi.org/10.1093/molbev/msw054
Kutschera, U. (1988) A new leech species from North America, Helobdella californica nov. sp. (Hirudinea: Glossiphoniidae). Zoologischer Anzeiger, 220, 173–178.
Kvist, S., Oceguera-Figueroa, A., Siddall, M.E. & Erséus, C. (2010) Barcoding, types and the Hirudo files: using information content to critically evaluate the identity of DNA barcodes. Mitochondrial DNA, 21, 198–205.
https://doi.org/10.3109/19401736.2010.529905
Lai, Y., Chang, C. & Chen, J. (2009) Two new species of Helobdella Blanchard 1896 (Hirudinida: Rhynchobdellida) from Taiwan, with a checklist of hirudofauna of the island. Zootaxa, 2068 (1), 27–46.
https://doi.org/10.11646/zootaxa.2068.1.2
Lamarck, J.B. (1838) Histoire naturelle des animaux sans vertèbres : présentant les caractères généraux et particuliers de ces animaux , leur distribution , leurs classes , leurs familles , leurs genres, et la citation des principales espèces qui s’y rapportent : précédée. J. B. Bail. Paris, 665 pp.
https://doi.org/10.5962/bhl.title.46287
Lanfear, R., Calcott, B., Ho, S.Y.W. & Guindon, S. (2012) PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701.
https://doi.org/10.1093/molbev/mss020
Light, J.E. & Siddall, M.E. (1999) Phylogeny of the Leech Family Glossiphoniidae Based on Mitochondrial Gene Sequences and Morphological Data. The Journal of Parasitology, 85, 815–823.
https://doi.org/10.2307/3285816
Linnaeus, C. (1758) Systema naturae per regna tria naturae :secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Vol. 1. Impensis Direct. Laurentii Salvii, Holmiae, 824 pp.
https://doi.org/10.5962/bhl.title.542
Marrone, F., Sacco, F., Kehlmaier, C., Arizza, V. & Arculeo, M. (2016) Some like it cold: The glossiphoniid parasites of the Sicilian endemic pond turtle Emys trinacris (Testudines, Emydidae), an example of “parasite inertia”?. Journal of Zoological Systematics and Evolutionary Research, 54, 60–66.
https://doi.org/10.1111/jzs.12117
Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. 2010 Gateway Computing Environments Workshop, New Orleans, Los Angeles, 14 November 2010, 1–8.
https://doi.org/10.1109/GCE.2010.5676129
Monquin-Tandon, A. (1846) Monographie de la famille des hirudinées. Baillière, Paris, 448 pp.
https://doi.org/10.5962/bhl.title.6598
Moore, J.P. (1939) Leeches (Hirudinea) from the Atlas Mountains of Morocco. Annals and Magazine of Natural History, Series 11, 3, 80–87.
https://doi.org/10.1080/03745481.1939.9723576
Moore, P.J. (1899) The leeches of the U. S. National Museum. Proceedings of the United States National Museum, 21, 543–563.
https://doi.org/10.5479/si.00963801.21-1160.543
Moore, P.J. (1911) Hirudinea of Southern Patagonia. Reports of the Princeton University Expeditions to Patagonia, 1896–1899, 3, 669–687.
Moser, W.E., Fend, S. V., Richardson, D.J., Hammond, C.I., Lazo-Wasem, E.A., Govedich, F.R. & Gullo, B.S. (2013) A new species of Helobdella (Hirudinida: Glossiphoniidae) from Oregon, USA. Zootaxa, 3718 (3), 287–294.
https://doi.org/10.11646/zootaxa.3718.3.5
Moser, W.E., Richardson, D.J., Hammond, C.I. & Lazo-Wasem, E. (2011) Molecular characterization of Helobdella modesta (Verrill, 1872) (Hirudinida: Glossiphoniidae) from its type locality, West River and Whitneyville Lake, New Haven County, Connecticut, USA. Zootaxa, 2834 (1), 65–68.
https://doi.org/10.11646/zootaxa.2834.1.6
Müller, O.F. (1774) Vermium terrestrium et fluviatilium, seu animalium infusoriorum, helminthicorum et testaceorum, non marinorum, succincta historia. Vol. 1. Heineck et Faber, Lipsiae, 72 pp.
https://doi.org/10.5962/bhl.title.12733
Müller, O.F. (1776) Zoologiae Danicae Prodromus, seu Animalium Daniae et Norvegiae Indigenarum Characteres, Nomina, et Synonyma Imprimis Popularium. Typis Hallageriis, Hafniae, 282 pp.
https://doi.org/10.5962/bhl.title.13268
Oceguera-Figueroa, A., León-Règagnon, V. & Siddall, M.E. (2005) Phylogeny and revision of Erpobdelliformes (Annelida, Arhynchobdellida) from Mexico based on nuclear and mitochondrial gene sequences. Revista Mexicana de Biodiversidad, 76, 191–198.
Oceguera-Figueroa, A. (2006) A new species of freshwater leech of the genus Haementeria (Annelida: Glossiphoniidae) from Jalisco State, Mexico. Zootaxa, 1110 (1), 39–45.
https://doi.org/10.11646/zootaxa.1110.1.4
Oceguera-Figueroa, A. (2012) Molecular phylogeny of the New World bloodfeeding leeches of the genus Haementeria and reconsideration of the biannulate genus Oligobdella. Molecular Phylogenetics and Evolution, 62, 508–514.
https://doi.org/10.1016/j.ympev.2011.10.020
Oceguera-Figueroa, A. & Leon-Regagnon, V. (2005) A new freshwater leech species of Helobdella (Annelida: Glossiphoniidae) from central Mexico. Zootaxa, 976 (1), 1–8.
https://doi.org/10.11646/zootaxa.976.1.1
Oceguera-Figueroa, A., León-Reògagnon, V. & Siddall, M.E. (2010) DNA barcoding reveals Mexican diversity within the freshwater leech genus Helobdella (Annelida: Glossiphoniidae). Mitochondrial DNA, 21, 24–29.
https://doi.org/10.3109/19401736.2010.527965
Oka, A. (1930) Sur un nouveau genre d’ Hirudinees provenant de l’Amérique du Sud. Proceedings of the Imperial Academy, Tokyo, 6, 239–242.
https://doi.org/10.2183/pjab1912.6.239
Oken, L. (1815) Lehrbuch Der Naturgeschichte. Dritter Theil. Zoologie. Thiere. and Atlas, Fleischlose, 850 pp.
Pennant, T., White, B. & Adams, E. (1768) British zoology. Vol. 4. Wilkie and Robinson, London, 380 pp.
https://doi.org/10.5962/bhl.title.62499
Reid, G.M.G. (2009) Carolus Linnaeus (1707–1778): His life, philosophy and science and its relationship to modern biology and medicine. Taxon, 58, 18–31.
https://doi.org/10.1002/tax.581005
Richardson, D.J. (2017) Host associations of Helobdella octatestisaca (Hirudinida: Glossiphoniidae) and the first report of this leech in the United States. Comparative Parasitology, 84, 12–20.
https://doi.org/10.1654/1525-2647-84.1.18
Ringuelet, R. (1972) Algunos Hirudineos Del Muséum D’histoire Naturelle De Paris. Physis, 21, 93–103.
Ringuelet, R. (1985) Fauna de agua dulce de la República Argentina. Fundacion para la Educacion, la Ciencia y la Cultura, Buenos Aires, 321 pp.
Ringuelet, R.A. (1949) Notas sobre Hirudíneos Neotropicales VI: Presencia del Género Glossiphonia en la Argentina y Otras Adiciones al Conocimiento de la Hirudofauna de los Países del Plata. Notas del Museo de la Plata, 14, 141–159.
Saglam, N., Kutschera, U., Saunders, R., Saidel, W.M., Balombini, K.L.W. & Shain, D.H. (2018) Phylogenetic and morphological resolution of the Helobdella stagnalis species-complex (Annelida: Clitellata: Hirudinea). Zootaxa, 4403 (1), 61–86.
https://doi.org/10.11646/zootaxa.4403.1.3
Salas-Montiel, R., Phillips, A.J., De Leon, G.P.P. & Oceguera-Figueroa, A. (2014) Description of a new leech species of Helobdella (Clitellata: Glossiphoniidae) from Mexico with a review of Mexican congeners and a taxonomic key. Zootaxa, 3900 (1), 77–94.
https://doi.org/10.11646/zootaxa.3900.1.4
Šapkarev, J.A. (1970) The Fauna of Hirudinea of Macedonia. The taxonomy and distribution of leeches of Aegean Lakes. International Revue der gesamten Hydrobiologie und Hydrographie, 55, 317–324.
https://doi.org/10.1002/iroh.19700550303
Savigny, J.C. (1809) Système des Annelides. Description de l’Égypte, ou, Recueil des observations et des recherches qui ont ét faites en Égypte pendant l’expédition de l’armée française, 1, 108–120.
Sawyer, R.T. (1986) Leech Biology and Behavior. Claredon Press, Oxford, 1065 pp.
Scharff, R.F. (1898) The Irish Freshwater Leeches. The Irish Naturalist, 7, 188–194.
Sciacchitano, I. (1967) Leeches (Hirudinea) from Ethiopia. Journal of Natural History, 1, 189–194.
https://doi.org/10.1080/00222936700770201
Shankland, M., Bissen, S.T. & Weisblat, D.A. (1992) Description of the Californian leech Helobdella robusta sp. nov., and comparison with Helobdella triserialis on the basis of morphology, embryology, and experimental. Canadian Journal of Zoology, 70, 1258–63.
https://doi.org/10.1139/z92-174
Siddall, M.E. (2001a) Hirudinea from the Apolobamba in the Bolivian Andes, Including Three New Species of Helobdella (Clitellata: Hirudinea). American Museum Novitates, 3341, 1–14.
https://doi.org/10.1206/0003-0082(2001)341<0001:HFTAIT>2.0.CO;2
Siddall, M.E. (2001b) Leeches of Leguna Volcan, Bolivia, Including a New Species of Helobdella (Clitellata: Hirudinea). American Museum Novitates, 3313, 1–11.
https://doi.org/10.1206/0003-0082(2001)313<0001:LOLVNB>2.0.CO;2
Siddall, M.E. & Borda, E. (2003) Phylogeny and revision of the leech genus Helobdella (Glossiphoniidae) based on mitochondrial gene sequences and morphological data and a special consideration of the triserialis complex. Zoologica Scripta, 32, 23–33.
https://doi.org/10.1046/j.1463-6409.2003.00098.x
Siddall, M.E. & Borda, E. (2004) Leech Collections from Chile Including Two New Species of Helobdella (Annelida: Hirudinida). American Museum Novitates, 3457, 1.
https://doi.org/10.1206/0003-0082(2004)457<0001:LCFCIT>2.0.CO;2
Siddall, M.E. & Budinoff, R.B. (2005) DNA-barcoding evidence for widespread introductions of a leech from the South American Helobdella triserialis complex. Conservation Genetics, 6, 467–472.
https://doi.org/10.1007/s10592-005-4986-y
Stamatakis, A. (2014) RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313.
https://doi.org/10.1093/bioinformatics/btu033
Templeton, R. (1936) A catalogue of the species of Annulose Animals, and of Rayed Ones, found in Ireland, as selected from the Papers of the late J. Templenton, Esq., of Cranmore, with Localities, Descriptions, and Illustrations. The Magazine of Natural History and Journal of Zoology, Botany, Mineralogy, Geology, and Meteorology, 9, 233–243.
Tiberti, R. & Gentilli, A. (2010) First report of freshwater leech Helobdella stagnalis (Rhyncobdellida: Glossiphoniidae) as a parasite of an anuran amphibian. Acta Herpetologica, 5, 255–258.
https://doi.org/10.13128/Acta_Herpetol-9034
Turton, W. (1807) The british fauna. J. Evans, Swansea, 230 pp.
Verrill, A.E. (1872) Descriptions of North American freshwater leeches. American Journal of Science 3, 126–139.
https://doi.org/10.2475/ajs.s3-3.14.126
Verrill, A.E. (1874) Synopsis of the North American fresh-water leeches. Report of the U.S. Commission for Fish and Fisheries, 2, 666–689.
Zimić, A. (2015) Commensalism, Predation or Parasitism: First report of the leech Helobdella stagnalis Linnaeus, 1758 on yellow-bellied toad, Bombina variegata (Linnaeus, 1758). Ecologica Montenegrina, 9744, 62–63.