Abstract
Myzobdella lugubris is a commensal leech on crustaceans and a parasite to fishes, surviving predominantly in brackish waters throughout North America. Specimens in this study were collected within the tidal zone of the Delaware River basin (New Jersey and Pennsylvania). To compare regional M. lugubris specimens, defined characters were scored after dorsal and ventral dissections, and phylogenetic relationships were resolved using cytochrome c oxidase subunit 1 (CO1), 12S ribosomal RNA (rDNA) and 18S rDNA gene fragments. Variance between regional populations was low, suggesting recent dispersal events and/or strong evolutionary constraints. The reproductive biology of M. lugubris was explored by quantitative analysis of secreted cocoons. Specimens produced 32.67 ± 4.50 cocoons with fertilization ratios of 88.1% and hatching times of 48 ± 7 days at 17°C under laboratory conditions. At 22°C, 46 ± 28 cocoons were produced with fertilization ratios of 70.27% and hatching times of 28 ± 5 days. Surprisingly, each cocoon supported only one embryo, which is unusual among oligochaetes.
Acknowledgements
We thank Leo Sheng of the Extreme Philly Fishing Group for assistance with collections, and Paul Callomon for assistance with specimen deposition at the Academy of Natural Sciences in Philadelphia, PA. Supported by The Scientific and Technological Research Council of Turkey (TUBITAK) to NS and Busch Biomedical, GAIA and NSF DBI-0216233 grants to DHS.
References
Amin O.M. 1981. Leeches (Hirudinea) from Wisconsin, and the description of the spermatophore of Placobdella ornate. Transactions of the American Microscopical Society, 100, 42–51. 10.2307/3225782Search in Google Scholar
Anisimova M., Gascuel O. 2006. Approximate likelihood ratio test for branchs: A fast, accurate and powerful alternative. Systematic Biology, 55, 539–52. 10.1080/10635150600755453Search in Google Scholar
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. 10.1006/mpev.1999.0639Search in Google Scholar PubMed
Appy R.G., Cone D.K. 1982. Attachment of Myzobdella lugubris (Hirudinea: Piscicolidae) to Logperch, Percina caprodes, and Brown Bullhead, Ichtalurus nebulosus. Transactions of the American Microscopical Society, 101, 135–141. 10.2307/3225766Search in Google Scholar
Becker D.A., Heard R.G., Holmes P.D. 1966. A preimpoundment survey of the helminth and copepod parasites of Micropterus spp. of Beaver Reservoir in northwest Arkansas. Transactions of the American Fisheries Society, 95, 23–34. 10.1577/1548-8659(1966)95[23:APSOTH]2.0.CO;2Search in Google Scholar
Becker C.D., Dauble D.D. 1979. Records of Piscivorus Leeches (Hirudinea) from The Central Columbia River, Washington State. Fishery Bulletin, 76, 926–931Search in Google Scholar
Borda E., Siddall M.E. 2004a. Arhynchobdellida (Annelida: Oligochaeta: Hirudinida) phylogenetic relationships and evolution. Molecular Phylogenetics and Evolution, 30, 213–225. 10.1016/j.ympev.2003.09.002Search in Google Scholar
Borda E., Siddall M.E. 2004b. Review of the evolution of life history strategies and phylogeny of the Hirudinida (Annelida: Oligochaeta). Lauterbornia, 52, 5–25Search in Google Scholar
Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Phylogenetics and Evolution, 17, 540–552. 10.1093/oxfordjournals.molbev.a026334Search in Google Scholar
Chevenet F., Brun C., BanulsAL., Jacq, B., Chisten R. 2006. Tree-Dyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics, 7, 439. 10.1186/1471-2105-7-439Search in Google Scholar PubMed
Daniels B.A., Sawyer R.T. 1975. The biology of the leech Myzobdella lugubris infesting blue crabs and catfish. Biological Bulletin, 148, 193–198. 10.2307/1540542Search in Google Scholar
Edgar R.C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 19, 1792–179710.1093/nar/gkh340Search in Google Scholar
Font W.F. 2003.The Global Spread of Parasites: What Do Hawaiian Streams Tell Us? BioScience, 53, 1061–1067. 10.1641/0006-3568(2003)053[1061:TGSOPW]2.0.CO;2Search in Google Scholar
Friend M. 1999. Nasal Leeches. Chapter 34. In: Friend, M. & Franson, J.C. (Eds). Field manual of wildlife diseases: general field procedures and diseases of birds. Madison, WI: US Geol. Survey, National Wildlife Health Center. pp. 245–92Search in Google Scholar
Goloboff P.A., Farris J.S., Nixon K.C. 2008. TNT, a free program for phylogenetic analysis. Cladistics, 24, 774–786. 10.1111/j.1096-0031.2008.00217.xSearch in Google Scholar
Guindon S., Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704. 10.1080/10635150390235520Search in Google Scholar PubMed
Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98Search in Google Scholar
Higgins D., Thompson J., Gibson T., ThompsonJ.D., Higgins, D.G., Gibson T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680. 10.1093/nar/22.22.4673Search in Google Scholar PubMed
Klemm D. J. 1972. Biota of Freshwater Ecosystems Identification Manual No 8. The leeches (Annelida: Hirudinea) of North America. Environmental Protection Agency Project No 18050ELD. The University of Michigan, Ann Arbor, Michigan. pp. 53Search in Google Scholar
Klemm D.J. 1982. The leeches (Annelida: Hirudinea) of North America. Cincinnati, Aquatic Biology Section, Environmental Monitoring and Support Laboratory, United States Environmental Protection AgencySearch in Google Scholar
Klemm D.J. 1985. Freshwater leeches (Annelida: Hirudinea). In Klemm DJ, editor. A guide to freshwater Annelida (Polychaeta, naidid and tubificid Oligochaeta, and Hirudinea) of North America. Dubuque: Kendall Hunt Publishing Co. pp. 198Search in Google Scholar
Klemm D.J. 1995. Identification guide to the freshwater leeches (Annelida: Hirudinea) of Florida and other southern states. Tallahassee: Florida Department of Environmental Protection. pp. 82Search in Google Scholar
Kutschera U., Wirtz P. 2001. The evolution of parental care in freshwater leeches. Theory in Biosciences, 120, 115–137. 10.1007/s12064-001-0012-1Search in Google Scholar
Kutschera U. 2016. Sex versus gender in sea urchins and leeches two centuries after Lamarck 1816. Journal of Marine Science: Research and Development, 6/5:1–310.4172/2155-9910.1000210Search in Google Scholar
Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. 2007. ClustalW and ClustalX, version 2. Bioinformatics, 23 2947–2948. 10.1093/bioinformatics/btm404Search in Google Scholar
Mason T.A., McIlroy P.J., Shain D.H. 2004. A cysteine-rich protein in the Theromyzon (Annelida: Hirudinea) cocoon membrane. Febs Letters, 561, 167–172. 10.1016/S0014-5793(04)00167-XSearch in Google Scholar PubMed
Mason T.A., Sayers C.W., Paulson T.L., Coleman J., Shain D.H. 2005. Cocoon deposition and hatching in the aquatic leech, Theromyzon tessulatum (Annelida, Hirudinea, Glossiphoniidae). American Midland Naturalist, 154, 78–87. 10.1674/0003-0031(2005)154[0078:Cdahit]2.0.Co;2Search in Google Scholar
Meyer M.C. 1940. A revision of the leeches (Piscicolidae) living on fresh-water fishes in North America. Transactions of the American Microscopical Society 59, 354–376. 10.2307/3222552Search in Google Scholar
Meyer M.C. 1946. Further notes on the leeches (Piscicolidae) living on fresh-water fishes of North America. Transactions of the American Microscopical Society 65, 237–249. 10.2307/3223419Search in Google Scholar PubMed
Moore J.P. 1946. The anatomy and systematic position of Myzobdella lugubris Leidy (Hirudinea). Notulae naturae of the Academy of Natural Sciences of Philadelphia, 184, 1–12Search in Google Scholar
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, 84–95Search in Google Scholar
Noga E.J., Bullis R.A., Miller G.C. 1990. Epidemic oral ulceration in largemouth bass (Micropterus salmoides) associated with the leech Myzobdella lugubris. Journal Wildlife Diseases, 26, 132–134. 10.7589/0090-3558-26.1.132Search in Google Scholar PubMed
Posada D., Buckley T.R. 2004. Model selection and model averaging in phylogenetics: advantages of Akaike Information Criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology, 53, 793–808. 10.1080/10635150490522304Search in Google Scholar PubMed
Posada D., Crandall K.A. 1998. Modeltest: testing the modelof DNA substitution. Bioinformatics, 14, 817–818. 10.1093/bioinformatics/14.9.817Search in Google Scholar PubMed
Rambaut A. 2016. FigTree v1.4.2; Molecular evolution, phylogenetics and epidemiology. http://tree.bio.ed.ac.uk/software/figtree/Search in Google Scholar
Ronquist F., Huelsenbeck J. and Teslenko M. 2011. Draft MrBayes version 3.2 Manual: Tutorials and Model Summaries. pp. 172Search in Google Scholar
Ronquist F., Huelsenbeck J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574. 10.1093/bioinformatics/btg180Search in Google Scholar PubMed
Rossi A.M., Saidel W.M., Marotta R., Saglam N., Shain D.H. 2013. Operculum ultrastructure in leech cocoons. Journal Morphology, 274, 940–946. 10.1002/jmor.20150Search in Google Scholar PubMed
Rossi A.M, Saidel W.M., Gravante C., Sayers C.W., Shain D.H. 2016. Mechanics of cocoon secretion in a segmented worm (Annelida: Hirudinidae). Micron, 86, 30–35. 10.1016/j.micron.2016.04.004Search in Google Scholar PubMed
Sambrook J., Russell, D.W. 2001. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New YorkSearch in Google Scholar
Sawyer R.T. 1972. North American freshwater leeches, exclusive of the Piscicolidae, with a key to all Species. University of Illinois Press, Urbana, Chicago and New York10.5962/bhl.title.53881Search in Google Scholar
Sawyer R.T. 1986. Leech Biology and Behavior. Vol. 1–3. Oxford University Press, New YorkSearch in Google Scholar
Sawyer R.T., Lawler A.R., Overstreet R. M. 1975. Marine leeches of the eastern United States and the Gulf of Mexico with a key to the species. Journal of Natural History, 9, 633–667. 10.1080/00222937500770531Search in Google Scholar
Sawyer R.T., Shelley R.M. 1976. New records and species of leeches (Annelida: Hirudinea) from North and South Carolina. Journal of Natural History, 10, 65–97. 10.1080/00222937600770061Search in Google Scholar
Sayers C.W., Coleman J., Shain D.H. 2009. Cell dynamics during cocoon secretion in the aquatic leech, Theromyzon tessulatum (Annelida: Clitellata: Glossiphoniidae). Tissue Cell, 41, 35–42. 10.1016/j.tice.2008.05.003Search in Google Scholar PubMed
Schramm J.C., Hardman C.H., Tarter D.C. 1981. The occurrence of Myzobdella lugubris and Piscicolaria reducta (Hirudinea: Piscicolidae) on fishes from West Virginia. Transactions of the American Microscopical Society, 100, 427–428. 10.2307/3226158Search in Google Scholar
Siddall M. E., Burreson E.M. 1995. Phylogeny of the Euhirudinea: Independent evolution of blood feeding by leeches? Canadian Journal of Zoology, 73, 1048–1064. 10.1139/z95-125Search in Google Scholar
Trauger D.L., Bartonek J.C. 1977. Leech parasitism of waterfowl in North America: Wildfowl, 28, 142–152Search in Google Scholar
Troxel, D.J., 2010. Parasites of Largemouth Bass (Micropterus salmoides) in Northern California. A Thesis Presented to The Faculty of Humboldt State University In Partial Fulfillment of The Requirements for the Degree Masters of Science Natural Resources, Fisheries, pp.59Search in Google Scholar
Utevsky S., Trontelj P. 2004. Phylogenetic relationships offish leeches (Hirudinea, Piscicolidae) based on mitochondrial DNA sequences and morphological data. Zoologica Scripta 33, 375–385. 10.1111/j.0300-3256.2004.00156.xSearch in Google Scholar
Wilkialis J., Davies R.W. (1980) The Reproductive-Biology of Theromyzon tessulatum (Glossiphoniidae-Hirudinoidea), with Comments on Theromyzon rude. Journal Zoology, 192, 421–429. 10.1111/j.1469-7998.1980.tb04241.xSearch in Google Scholar
Williams J. I., Burreson E.M. (2006). Phylogeny of the fish leeches (Oligochaeta, Hirudinida, Piscicolidae) based on nuclear and mitochondrial genes and morphology. Zoologica Scripta, 35, 627–639. 10.1111/j.1463-6409.2006.00246.xSearch in Google Scholar
Williams Jr., E.H., Bunkley-Williams L., Burreson E.M. (1994) Some New Records of Marine and Freshwater Leeches from Caribbean, Southeastern U.S.A., Eastern Pacific, and Okinawan Animals. Journal of The Helminthological Society of Washington, 61, 133–138Search in Google Scholar
Wirchansky B.A., Shain D.H. 2010. A new species of Haemopis (Annelida: Hirudinea): Evolution of North American terrestrial leeches. Molecular Phylogenetics and Evolution, 54, 226–234. 10.1016/j.ympev.2009.07.039Search in Google Scholar PubMed
Wrona F.J., Linton L.R., Davies R.W. 1987 Reproductive success and growth of two species of Erpobdellidae: the effect of water temperature. Canadian Journal of Zoology, 65, 1253– 1256. 10.1139/z87-195Search in Google Scholar
© 2018 W. Stefański Institute of Parasitology, PAS
