Home Phylogeny and cocoon production in the parasitic leech Myzobdella lugubris Leidy, 1851 (Hirudinidae, Piscicolidae)
Article
Licensed
Unlicensed Requires Authentication

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

  • Naim Saglam , Ralph Saunders , Shirley A. Lang and Daniel H. Shain EMAIL logo
Published/Copyright: January 17, 2018
Become an author with De Gruyter Brill

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

Received: 2017-4-6
Revised: 2017-9-19
Accepted: 2017-9-21
Published Online: 2018-1-17
Published in Print: 2018-3-26

© 2018 W. Stefański Institute of Parasitology, PAS

Articles in the same Issue

  1. Invited Paper
  2. Ultrastructure of digenean trematode eggs (Platyhelminthes: Neoophora): A review emphasizing new comparative data on four European Microphalloidea
  3. Phylogeny and cocoon production in the parasitic leech Myzobdella lugubris Leidy, 1851 (Hirudinidae, Piscicolidae)
  4. Parasites in stray dogs from Italy: prevalence, risk factors and management concerns
  5. A serological study of antibodies to Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato in the sera of healthy individuals collected two decades apart
  6. Changes in the incidence of intestinal giardiosis in Mexican population during five years (2011-2015)
  7. Molecular target analysis of stearoyl-CoA desaturase genes of protozoan parasites
  8. Molecular and morphological characterisation of Rhabdias picardiae Junker, Lhermitte-Vallarino et Bain, 2010 (Nematoda: Rhabdiasidae) from Delaland’s River Frog, Amietia delalandii (Duméril et Bibron, 1841) (Amphibia: Pyxicephalidae) in South Africa
  9. Scanning electron microscopy study of Strabax monstrosus von Nordmann, 1864 (Copepoda: Chondracanthidae) from Tunisian waters and histopathological study of its effects on host
  10. Characterization of phosphate transporter(s) and understanding their role in Leishmania donovani parasite
  11. Two nematode species from freshwater and marine fishes in Thailand, including Ascarophis scatophagi sp. nov. (Cystidicolidae) from Scatophagus argus (Scatophagidae)
  12. Metazoan parasite fauna of migrating common garfish, Belone belone (L.), in the Baltic Sea
  13. Measurement of binding strength between prey proteins interacting with Toxoplasma gondii SAG1 and SAG2 using isothermal titration calorimetry (ITC)
  14. Asymmetric peptidomimetics containing L-tartaric acid core inhibit the aspartyl peptidase activity and growth of Leishmania amazonensis promastigotes
  15. Transcriptional analysis of immune-relevant genes in the mucus of Labeo rohita, experimentally infected with Argulus siamensis
  16. Prevalence of endoparasitic infections of birds in zoo gardens in Serbia
  17. Contamination of swimming pools and hot tubs biofilms with Acanthamoeba
  18. Morphological and molecular characterization of Seuratascaris numidica (Seurat, 1917) (Ascaridida: Ascarididae)
  19. Nematode Thelazia callipaeda is spreading across Europe. The first survey of red foxes from Slovakia
  20. A frequent roundworm Baylisascaris transfuga in overpopulated brown bears (Ursus arctos) in Slovakia: a problem worthy of attention
  21. Nematode parasites of Duttaphrynus stomaticus (Lutken, 1864) (Amphibia: Anura) with description of a new species of Rhabdias Stiles and Hassall, 1905 (Nematoda: Rhabdiasidae) from Dehradun (Uttarakhand), India
  22. Molecular and serological investigation of infectious diseases in captive and free-range crab-eating fox (Cerdocyon thous – Linnaeus, 1776) from northeastern Brazil
  23. A new species of Aplectana (Nematoda, Cosmocercidae) in Goniurosaurus bawanglingensis (Squamata, Eublepharidae), from Hainan Province, China
  24. Syphacia muris infection in rats attenuates colorectal carcinogenesis through oxidative stress and gene expression alterations. Implications for modulatory effects by Bryostatin-1
  25. Research Note
  26. The first case of Leporacarus gibbus infestation in a rabbit from Poland
  27. Research Note
  28. Pathological and molecular studies of the renal trematode Paratanaisia bragai in Indian peafowls (Pavo cristatus)
Downloaded on 24.9.2025 from https://www.degruyterbrill.com/document/doi/10.1515/ap-2018-0002/html?lang=en
Scroll to top button