Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 4403 No. 1: 3 Apr. 2018
Type: Article
Published: 2018-04-03
DOI: 10.11646/zootaxa.4403.1.3
Page range: 61–86
Abstract views: 123
PDF downloaded: 3

Phylogenetic and morphological resolution of the Helobdella stagnalis species-complex (Annelida: Clitellata: Hirudinea)

Dept. of Aquaculture and Fish Diseases, Fisheries Faculty, Firat University, 23119 Elazig, Turkey
Institute of Biology, University of Kassel, 34132 Kassel, Heinrich-Plett Str. 40, Germany
Biology Department, Rutgers The State University of New Jersey, 315 Penn Street, Camden, NJ 08102, USA
Biology Department, Rutgers The State University of New Jersey, 315 Penn Street, Camden, NJ 08102, USA
Biology Department, Rutgers The State University of New Jersey, 315 Penn Street, Camden, NJ 08102, USA
Biology Department, Rutgers The State University of New Jersey, 315 Penn Street, Camden, NJ 08102, USA
Annelida leech Hirudinea scute COI

Abstract

The glossiphoniid freshwater leech, Helobdella stagnalis, was described by Linnaeus 1758 based on common European specimens. The presence of a brown, chitinous scute on the dorsal-anterior surface, as observed on leeches elsewhere in the world, has generally led to the classification of all scute-bearing members of the genus as H. stagnalis. Here we describe the morphology and behavior of the type species from Europe, and analyze H. stagnalis-like specimens collected worldwide. We present evidence for at least four distinct scute-bearing Helobdella species that can be morphologically resolved. Maximum Parsimony (MP) and Bayesian Inference (BI) analyses at the mitochondrial cytochrome c oxidase subunit I (COI) locus further supported this notion, with divergence values suggesting a mid-Miocene ancestor of this successful group of cosmopolitan hirudineans. New species, Helobdella echoensis nov. sp., Helobdella eriensis nov. sp., and Helobdella serendipitious nov. sp., are described, based on morphological, anatomical and molecular data. Current distribution patterns of Helobdella spp. suggest a robust, global dispersal mechanism, as well as local pockets of endemism.

 

References

  1. Apakupakul, K., Siddall, M.E. & Burreson, E.M. (1999) Higher level relationships of leeches (Annelida : Clitellata : Euhirudinea) based on morphology and gene sequences. Molecular Phylogenetics and Evolution, 12, 350–359.
    https://doi.org/10.1006/mpev.1999.0639

    Bely, A. & Weisblatt D.A. (2006) Lessions from leeches: a call for DNA barcoding in the lab. Evolution and Development, 8, 491–591.
    https://doi.org/10.1111/j.1525-142X.2006.00122.x

    Ben Ahmed, R., Romdhane, Y. & Tekaya, S. (2015a) Checklist and Distribution of Marine and freshwater leeches (Annelida, Clitellata, Hirudinea) in Tunisia with identification key. Ecologica Montenegrina, 2, 3–19.

    Ben Ahmed, R.B., Gammoudi, M., Khaled, I., Tekaya, S., Mansour, L., Alwasel, S. & Harrath, A.H. (2015b) Annotations on marine and freshwater leeches (Annelida, Clitellata, Hirudinea) from North Africa. Tropical Zoology, 23, 71–93.
    https://doi.org/10.1080/03946975.2015.1046737

    Blanchard, R. (1896) Viaggio del dott. A. Borelli nella Republica Argentina e nel Paraguay XXI. Hirudinees. Bolletino Museum Zoologia et Anatomia Comparativa Torino, 11,1–24.

    Borda, E. & Siddall, M.E. (2004a) Phylogeny and evolution of the Arhynchobdellida (Annelida: Oligochaeta: Hirudinida). Cladistics - The International Journal of the Willi Hennig Society, 20, 77–78.

    Borda, E. & Siddall, M.E. (2004b) Arhynchobdellida (Annelida: Oligochaeta: Hirudinida): phylogenetic relationships and evolution. Molecular Phylogenetics and Evolution, 30, 213–225.
    https://doi.org/10.1016/j.ympev.2003.09.002

    Chordas, S.W., Harp, G.L. & Wolfe, G.W. (1996) The aquatic macroinvertebrates of the White River National Wildlife Refuge, Akansas. Proceedings of the Arkansas Academy of Science, 50, 42–51.

    Christoffersen, M. (2009) A catalogue of Helobdella (Annelida, Clitellata, Hirudinea, Glossiphoniidae), with a summary of leech diversity, from South America. Neotropical Biology and Conservation, 4, 89–98.
    https://doi.org/10.4013/nbc.2009.42.04

    Cochran, B.G. & Harp, G.L. (1990) The aquatic macro-invertebrates of the St. Francis Sunken Lands in northeast Arkansas. Proceedings of the Arkansas Academy of Science, 44, 23–27.

    Curry, M.G. (1976) Three leeches (Hirudinea) new to Arkansas with ecological and distribution notes. Wasmann Journal of Biology, 34, 5–8.

    Davy, C.M., Shim, K.C. & Coombes, S.M. (2009) Leech (Annelida: Hirudinea) infestations on canadian turtles, including the first canadian record of Helobdella modesta from freshwater turtles. Canadian Field-Naturalist, 123, 44–47.
    https://doi.org/10.22621/cfn.v123i1.673

    Dial, C.R., Dial, R.J., Saunders, R., Lang, S.A., Tetreau, M.D., Lee, B., Wimberger, P., Dinapoli, M.S., Egiazarov, A.S., Gipple, S.L., Maghirang, M.R., Swartley-McArdle, D.J., Yudkovitz, S.R. & Shain, D.H. (2012) Historical biogeography of the North American glacier ice worm, Mesenchytraeus solifugus (Annelida: Oligochaeta: Enchytraeidae). Molecular Phylogenetics and Evolution, 63, 577–584.
    https://doi.org/10.1016/j.ympev.2012.01.008

    Ermak, T.H. & Eakin, R.M. (1976) Fine structure of the cerebral and pygidial ocelli in Chone ecaudata (Polychaeta: Sabellidae). Journal of Ultrastructural Research, 54, 243–260.
    https://doi.org/10.1016/S0022-5320(76)80154-2

    Felsenstein, J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39, 783–791.
    https://doi.org/10.1111/j.1558-5646.1985.tb00420.x

    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

    Gouda, H.A. (2013) Spermatogenesis, spermiogenesis and sperm transfer in two freshwater leeches from Assiut, Egypt. Research in Zoology, 3, 45–55.

    Govedich, F.R., Bain, B.A., Moser, W.E., Gelder, S.R., Davies, R.W. & Brinkhurst, R.O. (2010) Annelida (Clitellata) Oligochaeta, Branchiobdellida, Hirudinida, and Acanthobdellida. In: Thorp, J.H., Covich, A.P. (Eds.), Ecology and Classification of North American Freshwater Invertebrates. Academic Press/Elsevier, San Diego, CA, pp. 385–436.
    https://doi.org/10.1016/B978-0-12-374855-3.00012-1

    Harp, G.L. & Harp, P.A. (1980). Aquatic macroinvertebrates of Wapanocca National Wildlife Refuge. Proceedings of the Arkansas Academy of Science, 34, 115–117.

    Hughes, S.J., Furse, M.T., Blackburn, J.H. & Langton, P.H. (1998) A Checklist of Madeiran Freshwater Macroinvertebrates. Boletim do Museu Municipal do Funchal, 50, 5–41.

    Klemm, D.J. (1972) Biota of Freshwater Ecosystems. Identification Manual No. 8. Freshwater Leeches (Annelida: Hirudinea) of North America. US Government Printing Office, Washington, D.C., 58 pp.

    Klemm, D.J. (1982) Leeches (Annelida: Hirudinea) of North America. Environmental Monitoring and Support Laboratory. U.S. Environmental Protection Agency, Cincinnati, OH, 200 pp. [OH 45268, EPA-600/3-82-025]

    Klemm, D.J. (1985) IdentificatiOn Guide To The Freshwater Leeches (Annelida: Hirudinea) Of Florida And Other Southern States. Florida Department of Environmental Protection, Tallahassee, Florida, 82 pp.

    Klemm, D.J. (1991) Taxonomy and pollution ecology of the great Lakes Region leeches (Annelida: Hirudinea). Michigan Academician, 24, 37–103.

    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

    Kuo, D.H. (2009) Annelids in Evolutionary Developmental Biology. In: Shain, D.H. (Ed.), Annelids in Modern Biology. John Wiley & Sons, Hoboken, NJ.
    https://doi.org/10.1002/9780470455203.ch5

    Kuo, D.H. & Weisblat, D.A. (2011) Intermediate filament genes as differentiation markers in the leech Helobdella. Development, Genes and Evolution, 221, 225–240.
    https://doi.org/10.1007/s00427-011-0375-3

    Kutschera, U. (1988) A new leech species from North-America, Helobdella californica nov. sp. (Hirudinea, Glossiphoniidae). Zoologischer Anzeiger, 220, 173–178.

    Kutschera, U. (2011). The Golden Gate Leech Helobdella californica (Hirudinea Glossiphoniidae): occurrence and DNA-based taxonomy of a species restricted to San Francisco. International Revue of Hydrobiology, 96, 286–295.
    https://doi.org/10.1002/iroh.201111311

    Kutschera, U. & Wirtz, P. (1986) A leech that feeds ist young. Animal Behaviour, 34, 941–942.
    https://doi.org/10.1016/S0003-3472(86)80087-2

    Kutschera, U. & Wirtz, P. (2001) The evolution of parental care in freshwater leeches. Theory in Biosciences, 120,115–137.
    https://doi.org/10.1007/s12064-001-0012-1

    Kutschera, U., Langguth, H., Kuo, D.-H., Weisblat, D.A. & Shankland, M. (2013) Description of a new leech species from North America, Helobdella austinensis n. sp. (Hirudinea: Glossiphoniidae), with observation on its feeding behaviour. Zoosystematics and Evolution, 89, 239–246.
    https://doi.org/10.1002/zoos.201300010

    Kutschera, U. & Weisblat, D.A. (2015). Leeches of the genus Helobdella as model organisms for Evo-Devo studies. Theory in Biosciences, 134, 93–104.
    https://doi.org/10.1007/s12064-015-0216-4

    Lai, Y.T., Chang, C.H. & Chen, J.H. (2009) Two new species of Helobdella Blanchard 1896 (Hirudinida: Rhynchobdellida: Glossiphoniidae) from Taiwan, with a checklist of hirudinea fauna of the island. Zootaxa, 2068, 27–46.

    Lanfear, R., Calcott, B., Ho, S. & 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

    Linnaeus C. (1758) Systema Naturae per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, cum Characteribus Differentiis Synomymis Locis. Tomus I. 10th Edition. Impensis Direct. Laurentii Salvii, Holmiae, 824 pp.

    Maddison, W.P. & Maddison, D.R. (2015) Mesquite: a modular system for evolutionary analysis, Version 3.04. Available from: http://mesquiteproject.org (accessed 21 February 2018)

    Moore, J.P. (1906) Hirudinea and Oligochaeta collected in the Great Lakes region. Bureau of Fisheries Bulletin, 25 (598), 153–172.

    Moore, J.P. (1939) Leeches (Hirudinea) from the Atlas Mountains of Marocco. Annals and Magazine of Natural History, 3, 80–87.
    https://doi.org/10.1080/00222933908526901

    Moser, W.A. (1991) Leeches (Annelida: Hirudinea) in Central and Western Nebraska. Transactions of the Nebraska Academy of Sciences, 18, 87–91.

    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, 287–294.
    https://doi.org/10.11646/zootaxa.3718.3.5

    Moser, W.E., Klemm, D.J., Richardson, D.J., Wheeler, B.A., Trauth, S.E. & Daniels, B.A. (2006). Leeches (Annelida Hirudinida) of Northern Arkansas. Journal of the Arkansas Academy of Science, 60, 84–95.

    Nei, M. & Kumar, S. (2000) Molecular Evolution and Phylogenetics. Oxford University Press, New York, 333 pp.

    Oceguera-Figueroa, A., Kvist, S., Watson, C.S., Sankar, D.F., Overstreet, R.M. & Siddall, M.E. (2010a) Leech collections from Washington State, with the description of two new species of Placobdella (Annelida Glossiphoniidae). American Museum Novitatis, 3701, 1–14.
    https://doi.org/10.1206/3701.2

    Oceguera-Figueroa, A., Leon-Regagnon, V. & Siddall, M.E. (2010b) 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

    Oosthuizen, J.H. & Siddall, M.E. (2003) The Freshwater leeches (Hirudinea) of Southern Africa With a key to all species. In: Guide to Freshwater Invertebrates in Southern Africa. South African Water Research Commission, Pretoria, pp. 237–263.

    Pfeiffer, I., Brenig, B. & Kutschera, U. (2004) The occurence of an Australian leech species (genus Helobdella) in German freshwater habitats as revealed by mitochondrial DNA sequences. Molecular Phylogenetics and Evolution, 33, 214–219.
    https://doi.org/10.1016/j.ympev.2004.04.010

    Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
    https://doi.org/10.1093/bioinformatics/btg180

    Ronquist, F., Huelsenbeck, J. & Teslenko, M. (2011) Draft MrBayes version 3.2 Manual. Tutorials and Model Summaries. Available from: http://mrbayes.sourceforge.net/mb3.2_manual.pdf (accessed 21 February 2018)

    Saglam, N. & Dorucu, M. (2002) Observations on the ecology of the freshwater leech Helobdella stagnalis (Hirudinoidea: Glossiphoniidae), new for Turkey. Zoology in the Middle East, 25, 115–120.
    https://doi.org/10.1080/09397140.2002.10637912

    Salas-Montiel, R., Phillips, A.J., De Leon, G.P.P. & Oceguera-Fıgueroa, 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

    Sawyer, R.T. (1986) Leech Biology and Behavior. Vol. I–III. Clarendon Press, Oxford, xiv + 1065 pp.

    Sheehan, D. & Hrapchak B. (1980) Theory and Practice of Histotechnology. 2nd Edition. Battelle, Ohio, 841 pp. [pp. 189–190]

    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., Budinoff, R.B. & Borda, E. (2005) Phylogenetic evaluation of systematics and biogeography of the leech family Glossiphoniidae. Invertebrate Systematics, 19, 105–112.
    https://doi.org/10.1071/IS04034

    Sket, B. & Trontelj, P. (2008) Global diversity of leeches (Hirudinea) in freshwater. Hydrobiologia, 595, 129–137.
    https://doi.org/10.1007/s10750-007-9010-8

    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.

    Verrill A.E. (1872) Description of North American freshwater leeches. American Journal of Science, 3, 126–139.
    https://doi.org/10.2475/ajs.s3-3.14.126

    Young, J.O., Martin, A.J. & Seaby, R.M.H. (1993) Competitive interactions between the lake-dwelling leeches Glossiphonia complanata and Helobdella stagnalis: an experimental investigation of the significance of a food refuge. Oecologia, 93, 156–161.
    https://doi.org/10.1007/BF00317664