Acta Parasitologica

, Volume 63, Issue 1, pp 15–26 | Cite as

Phylogeny and cocoon production in the parasitic leech Myzobdella lugubris Leidy, 1851 (Hirudinidae, Piscicolidae)

  • Naim Saglam
  • Ralph Saunders
  • Shirley A. Lang
  • Daniel H. ShainEmail author


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.


Reproduction oligochaete channel catfish crustacean 


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  1. 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. DOI; 10.2307/3225782CrossRefGoogle Scholar
  2. Anisimova M., Gascuel O. 2006. Approximate likelihood ratio test for branchs: A fast, accurate and powerful alternative. Systematic Biology, 55, 539–52. DOI: 10.1080/10635150600755453CrossRefGoogle Scholar
  3. 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. DOI: 10.1006/mpev.1999.0639CrossRefGoogle Scholar
  4. 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. DOI: 10.2307/3225766CrossRefGoogle Scholar
  5. 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. DOI: 10.1577/1548-8659(1966)95[23:APSOTH]2.0.CO;2CrossRefGoogle Scholar
  6. Becker C.D., Dauble D.D. 1979. Records of Piscivorus Leeches (Hirudinea) from The Central Columbia River, Washington State. Fishery Bulletin, 76, 926–931Google Scholar
  7. Borda E., Siddall M.E. 2004a. Arhynchobdellida (Annelida: Oligochaeta: Hirudinida) phylogenetic relationships and evolution. Molecular Phylogenetics and Evolution, 30, 213–225. DOI 10.1016/j.ympev.2003.09.002CrossRefGoogle Scholar
  8. Borda E., Siddall M.E. 2004b. Review of the evolution of life history strategies and phylogeny of the Hirudinida (Annelida: Oligochaeta). Lauterbornia, 52, 5–25Google Scholar
  9. Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Phylogenetics and Evolution, 17, 540–552. DOI: 10.1093/ox-fordjournals.molbev.a026334Google Scholar
  10. Chevenet F., Brun C., Banuls AL., Jacq, B., Chisten R. 2006. Tree-Dyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics, 7, 439. DOI: 10.1186/1471-2105-7-439CrossRefGoogle Scholar
  11. Daniels B.A., Sawyer R.T. 1975. The biology of the leech Myzob-della lugubris infesting blue crabs and catfish. Biological Bulletin, 148, 193–198. DOI: 10.2307/1540542CrossRefGoogle Scholar
  12. Edgar R.C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 19, 1792–1797CrossRefGoogle Scholar
  13. Font W.F. 2003. The Global Spread of Parasites: What Do Hawaiian Streams Tell Us? BioScience, 53, 1061–1067. DOI: 10.1641/0006-3568(2003)053[1061:TGSOPW]2.0. CO;2CrossRefGoogle Scholar
  14. 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. 245–92Google Scholar
  15. Goloboff P.A., Farris J.S., Nixon K.C. 2008. TNT, a free program for phylogenetic analysis. Cladistics, 24, 774–786. DOI: 10.1111/j.1096-0031.2008.00217.xCrossRefGoogle Scholar
  16. Guindon S., Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704. DOI: 10.1080/10635150390235520CrossRefGoogle Scholar
  17. 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, 95–98Google Scholar
  18. Higgins D., Thompson J., Gibson T., Thompson J.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. DOI: 10.1093/nar/22.22.4673CrossRefGoogle Scholar
  19. 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. 53Google Scholar
  20. Klemm D.J. 1982. The leeches (Annelida: Hirudinea) of North America. Cincinnati, Aquatic Biology Section, Environmental Monitoring and Support Laboratory, United States Environmental Protection AgencyGoogle Scholar
  21. 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. 198Google Scholar
  22. 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. 82Google Scholar
  23. Kutschera U., Wirtz P. 2001. The evolution of parental care in freshwater leeches. Theory in Biosciences, 120, 115–137. DOI: 10.1007/s12064-001-0012-1CrossRefGoogle Scholar
  24. Kutschera U. 2016. Sex versus gender in sea urchins and leeches two centuries after Lamarck 1816. Journal of Marine Science: Research and Development, 6/5:1–3Google Scholar
  25. 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. DOI: 10.1093/bioinformatics/btm404CrossRefGoogle Scholar
  26. 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. DOI: 10.1016/S0014-5793(04) 00167-XCrossRefGoogle Scholar
  27. 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, Glossiphoni-idae). American Midland Naturalist, 154, 78–87. DOI: 10.1674/0003-0031(2005)154[0078:Cdahit]2.0.Co;2CrossRefGoogle Scholar
  28. 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. DOI: 10.2307/3222552CrossRefGoogle Scholar
  29. 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. DOI: 10.2307/ 3223419CrossRefGoogle Scholar
  30. Moore J.P. 1946. The anatomy and systematic position of Myzob-della lugubris Leidy (Hirudinea). Notulae naturae of the Academy of Natural Sciences of Philadelphia, 184, 1–12Google Scholar
  31. 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, 84–95Google Scholar
  32. 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. DOI: 10.7589/0090-3558-26.1.132CrossRefGoogle Scholar
  33. 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. DOI: 10.1080/1063515049052 2304CrossRefGoogle Scholar
  34. Posada D., Crandall K.A. 1998. Modeltest: testing the modelof DNA substitution. Bioinformatics, 14, 817–818. DOI: 10.1093/bioin-formatics/14.9.817CrossRefGoogle Scholar
  35. Rambaut A. 2016. FigTree v1.4.2; Molecular evolution, phylogenetics and epidemiology. Scholar
  36. Ronquist F., Huelsenbeck J. and Teslenko M. 2011. Draft MrBayes version 3.2 Manual: Tutorials and Model Summaries. pp. 172Google Scholar
  37. Ronquist F., Huelsenbeck J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574. DOI: 10.1093/bioinformatics/btg180CrossRefGoogle Scholar
  38. Rossi A.M., Saidel W.M., Marotta R., Saglam N., Shain D.H. 2013. Operculum ultrastructure in leech cocoons. Journal Morphology, 274, 940–946. DOI: 10.1002/jmor.20150CrossRefGoogle Scholar
  39. 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. DOI: 10. 1016/j.micron.2016.04.004CrossRefGoogle Scholar
  40. Sambrook J., Russell, D.W. 2001. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New YorkGoogle Scholar
  41. 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 YorkCrossRefGoogle Scholar
  42. Sawyer R.T. 1986. Leech Biology and behavior. Vol. 1–3. Oxford University Press, New YorkGoogle Scholar
  43. 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. DOI: 10.1080/00222937500770531CrossRefGoogle Scholar
  44. 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. DOI: 10.1080/00222937600770061CrossRefGoogle Scholar
  45. 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. DOI: 10.1016/j.tice.2008.05.003CrossRefGoogle Scholar
  46. Schramm J.C., Hardman C.H., Tarter D.C. 1981. The occurrence of Myzobdella lugubris and Piscicolaria reducta (Hirudinea: Pis-cicolidae) on fishes from West Virginia. Transactions of the American Microscopical Society, 100, 427–428. DOI: 10.2307/3226158CrossRefGoogle Scholar
  47. 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. DOI: 10.1139/z95-125CrossRefGoogle Scholar
  48. Trauger D.L., Bartonek J.C. 1977. Leech parasitism of waterfowl in North America: Wildfowl, 28, 142–152Google Scholar
  49. Troxel, D.J., 2010. Parasıtes of Largemouth Bass (Mıcropterus salmoıdes) 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.59Google Scholar
  50. Utevsky S., Trontelj P. 2004. Phylogenetic relationships offish leeches (Hirudinea, Piscicolidae) based on mitochondrial DNA sequences and morphological data. Zoologica Scripta 33, 375–385. DOI: 10.1111/j.0300-3256.2004.00156.xCrossRefGoogle Scholar
  51. Wilkialis J., Davies R.W. (1980) The Reproductive-Biology of Theromyzon tessulatum (Glossiphoniidae-Hirudinoidea), with Comments on Theromyzon rude. Journal Zoology, 192, 421–429. DOI: 10.1111/j.1469-7998.1980.tb04241.xCrossRefGoogle Scholar
  52. 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. DOI: 10.1111/j.1463-6409.2006.00246.xCrossRefGoogle Scholar
  53. 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, 133–138Google Scholar
  54. 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. DOI: 10.1016/j.ympev.2009.07.039CrossRefGoogle Scholar
  55. 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. DOI: 10.1139/z87-195CrossRefGoogle Scholar

Copyright information

© Witold Stefański Institute of Parasitology, Polish Academy of Sciences 2018

Authors and Affiliations

  • Naim Saglam
    • 1
  • Ralph Saunders
    • 2
  • Shirley A. Lang
    • 2
  • Daniel H. Shain
    • 2
    Email author
  1. 1.Dept. of Aquaculture and Fish Diseases, Fisheries FacultyFirat UniversityElazigTurkey
  2. 2.Biology DepartmentRutgers — The State University of New JerseyCamdenUSA

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