Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2025-04-29
Page range: 455-479
Abstract views: 50
PDF downloaded: 2

Species delimitation recovers undescribed Erpobdellidae (Annelida: Hirudinea) from USA and Türkiye

Dept. of Aquaculture and Fish Diseases; Fisheries Faculty; Firat University; 23119 Elazig; Türkiye
Biology Department; Rutgers The State University of New Jersey; 201 South Broadway; Camden; NJ 08103; USA
Annelida Clitellate Hirudinid Erpobdella morphology COI new species

Abstract

Erpobdellid leeches are morphologically similar to each other and thus cause confusion in taxonomic identification. In particular, annuli, colour and eye patterns are very close across species which creates difficulties in external morphological resolution. Here we describe six new species of Erpobdellidae collected from North America and Europe based on morphological and molecular criteria. New species are formally designated Erpobdella farmensis sp. nov., Erpobdella haddonensis sp. nov., Erpobdella madenensis sp. nov., Dina sivricensis sp. nov., Dina takasensis sp. nov. and Trocheta kesirvenensis sp. nov. Phylogenetic comparisons were conducted with fragments of nuclear (18S rRNA) and mitochondrial [12S rRNA and cytochrome c oxidase subunit I (COI)] loci to confirm species separation. A global phylogeny with all available data in GenBank at the COI locus identified 49 recognized erpobdellid species, many of which occur regionally or are distributed globally.

 

References

  1. Anderson, K., Braoudakis, G. & Kvist, S. (2020) Genetic variation, pseudocryptic diversity, and phylogeny of Erpobdella (Annelida: Hirudinida: Erpobdelliformes), with emphasis on Canadian species. Molecular phylogenetics and evolution, 143, 106688. https://doi.org/10.1016/j.ympev.2019.106688
  2. 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 (3), 350–359. https://doi.org/10.1006/mpev.1999.0639
  3. Ben Ahmed, R., Bielecki, A., Cichocka, J.M., Tekaya, S., Gorzel, M. & Harrath, A.H. (2013) Erpobdellid leeches (Annelida, Clitellata, Hirudinida) from Tunisia: new records with the description of a new Trocheta species. Zootaxa, 3681 (4), 440–54. https://doi.org/10.11646/zootaxa.3681.4.7
  4. Borda, E. & Siddall, M.E. (2004a) Arhynchobdellida (Annelida: Oligochaeta: Hirudinida): phylogenetic relationships and evolution. Molecular Phylogenetics and Evolution, 30 (1), 213–225. https://doi.org/10.1016/j.ympev.2003.09.002
  5. Borda, E. & Siddall, M.E. (2004b) Phylogeny and evolution of the Arhynchobdellida (Annelida: Oligochaeta: Hirudinida). Cladistics-the International Journal of the Willi Hennig Society, 20 (1), 77–78. https://doi.org/10.1016/j.ympev.2003.09.002
  6. Borda, E. & Siddall, M.E. (2004) Review of the evolution of life history strategies and phylogeny of the Hirudinida (Annelida: Oligochaeta). Lauterbornia, 52, 5–25.
  7. Bouckaert, R., Vaughan, T.G., Barido-Sottani, J., Duchêne, S., Fourment, M., Gavryushkina, A., Heled, J., Jones, G., Kühnert, D. & De Maio, N. (2019) BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS computational biology, 15 (4), e1006650. https://doi.org/10.1371/journal.pcbi.1006650
  8. Bunyard, B.A., Nicholson, M.S. & Royse, D.J. (1994) A systematic assessment of Morchella using RFLP analysis of the 28S ribosomal RNA gene. Mycologia, 86 (6), 762–772. https://doi.org/10.1080/00275514.1994.12026481
  9. Cichocka, J.M., Bielecki, A., Kur, J., Pikuła, D., Kilikowska, A. & Biernacka, B. (2015) A new leech species (Erpobdella) (Hirudinida: Erpobdellidae) from a cave in the West Azerbaijan province of Iran. Zootaxa, 4013 (3), 413–427. https://doi.org/10.11646/zootaxa.4013.3.5
  10. Darabi‐Darestani, K., Sari, A., Khomenko, A., Kvist, S. & Utevsky, S. (2021) DNA barcoding of Iranian leeches (Annelida: Clitellata: Hirudinida). Journal of Zoological Systematics and Evolutionary Research, 59 (7), 1438–1452. https://doi.org/10.1111/jzs.12538
  11. Dinno, A. & Dinno, M.A. (2018) Package ‘paran’. Dortmund, Germany: R package version, 1 (2). [program]
  12. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32 (5), 1792–1797. https://doi.org/10.1093/nar/gkh340
  13. Ezard, T., Fujisawa, T. & Barraclough, T.G. (2009) Splits: species’ limits by threshold statistics. R package version, 1 (11), r29.
  14. Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrıjenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome COX‐idase subunit 1 from diverse metazoan invertebrates. Molecular and Marine Biology Biotechnology, 3, 294–299.
  15. Fujisawa, T. & Barraclough, T.G. (2013) Delimiting species using single‐locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Systematic biology, 62 (5), 707–724. https://doi.org/10.1093/sysbio/syt033
  16. Grosser, C., Pešić, V., Berlajolli, V. & Gligorović, B. (2016) Glossiphonia balcanica n. sp. and Dina prokletijaca n. sp. (Hirudinida: Glossiphoniidae, Erpobdellidae)–two new leeches from Montenegro and Kosovo. Ecologica Montenegrina, 8, 17–26. https://doi.org/10.37828/em.2016.8.2
  17. Grosser, C., Rewicz, T., Jovanović, M., Zawal, A. & Pešić, V. (2023) Integrative taxonomy reveals a new species of the leech genus Dina R. Blanchard, 1892 (Annelida, Hirudinida: Erpobdellidae) from the ancient Skadar Lake basin in Montenegro. The European Zoological Journal, 90 (1), 383–394. https://doi.org/10.1080/24750263.2023.2216710
  18. 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, 95–98.
  19. Heled, J. (2015) Extended Bayesian skyline plot tutorial for BEAST 2. WWW document. Available from: http://evomicsorg.wpengine.netdna-cdn.com/wp-content (accessed 1 April 2025)
  20. 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 Res., 22, 4673–4680. https://doi.org/10.1093/nar/22.22.4673
  21. Kapli, P., Lutteropp, S., Zhang, J., Kobert, K., Pavlidis, P., Stamatakis, A. & Flouri, T. (2017) Multi‐rate Poisson tree processes for single‐locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics, 33 (11), 1630–1638. https://doi.org/10.1093/bioinformatics/btx025
  22. Khomenko, A., Utevsky, S., Utevsky, A. & Trontelj, P. (2020) Unrecognized diversity of Trocheta species (Hirudinea: Erpobdellidae): resolving a century‐old taxonomic problem in Crimean leeches. Systematics and Biodiversity, 18 (2), 129–141. https://doi.org/10.1080/14772000.2020.1739776
  23. Kimura, M. (1980) A Simple Method for Estimating Evolutionary Rates of Base Substitutions through Comparative Studies of Nucleotide‐Sequences. Journal of Molecular Evolution, 16 (2), 111–120. https://doi.org/10.1007/BF01731581
  24. Kosel, V. (2004) Taxonomical position of two species of Trocheta (Hirudinea) described from Central Europe. Biologia, 59, 25–28.
  25. Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Molecular Biology and Evolution, 35 (6), 1547–1549. https://doi.org/10.1093/molbev/msy096
  26. Kutschera, U. (2003) The feeding strategies of the leech Erpobdella octoculata (L.): A laboratory study. International Review of Hydrobiology, 88 (1), 94–101.
  27. Kutschera, U. (2010) A new leech species from Southern https://doi.org/10.1002/iroh.200390008 Germany, Trocheta intermedia nov. sp. (Hirudinea: Erpobdellidae). Lauterbornia, 70, 1–9.
  28. 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 (21), 2947–2948. https://doi.org/10.1093/bioinformatics/btm404
  29. Mann, K.H. (1952) A revision of the British leeches of the family Erpobdellidae with an account of Dina lineata (O. F. Müller, 1774), a leech new to the British fauna. Proceedings of the Zoological Society of London, 123, 377–391. https://doi.org/10.1111/j.1096-3642.1953.tb00180.x
  30. Medlin, L., Elwood, H.J., Stickel, S. & Sogin, M.L. (1988) The characterization of enzymatically amplified eukaryotic 16S‐like rRNA‐coding regions. Gene, 71 (2), 491–499. https://doi.org/10.1016/0378-1119(88)90066-2
  31. Michonneau, F., Bolker, B., Holder, M., Lewis, P. & O’Meara, B. (2018) Package ‘rncl’.
  32. Moser, W.E., Govedich, F.R., Oceguera‐Figueroa, A., Richardson, D.J. & Phillips, A.J. (2015) Subclass Hirudinida. In: Keys to Nearctic Fauna, Thorp and Covich’s Freshwater Invertebrates. Elsevier, pp. 244–259.
  33. Nei, M. & Kumar, S. (2000) Molecular Evolution and Phylogenetics. Oxford University Press, New York, New York, xiv + 333 pp. https://doi.org/10.1093/oso/9780195135848.001.0001
  34. Nesemann, H. & Neubert, E. (1999) Annelida: Clitellata: Branchiobdellida, Acanthobdellea, Hirudinea. Spektrum Akademischer Verlag, Heidelberg, Berlin, 178 pp.
  35. Nesemann, H. & Neubert, E. (1994) New data to the leeches of the subfamily Trochetinae (Hirudinea, Erpobdellidae). Miscellanea Zoologica Hungarica, 9, 19–28.
  36. Oceguera‐Figueroa, A., León‐Règagnon, V. & Siddall, M.E. (2005) Phylogeny and revision of Erpobdelliformes (Annelida, Arhynchobdellida) from Mexico based on nuclear and mithochondrial gene sequences. Revista mexicana de biodiversidad, 76 (2), 191–198. https://doi.org/10.22201/ib.20078706e.2005.002.307
  37. Oceguera‐Figueroa, A., Phillips, A.J., Pacheco‐Chaves, B., Reeves, W.K. & Siddall, M.E. (2011) Phylogeny of macrophagous leeches (Hirudinea, Clitellata) based on molecular data and evaluation of the barcoding locus. Zoologica Scripta, 40 (2), 194–203. https://doi.org/10.1111/j.1463-6409.2010.00465.x
  38. Paradis, E. (2012) Analysis of Phylogenetics and Evolution with R. 2nd Edition. Springer, New York, 400 pp. https://doi.org/10.1007/978-1-4614-1743-9
  39. Paradis, E. & Schliep, K. (2019) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics, 35 (3), 526–528. https://doi.org/10.1093/bioinformatics/bty633
  40. Pfeiffer, I., Brenig, B. & Kutschera, U. (2005) Molecular phylogeny of selected predaceous leeches with reference to the evolution of body size and terrestrialism. Theory Biosci, 124 (1), 55–64. https://doi.org/10.1016/j.thbio.2005.05.002
  41. Puillandre, N., Brouillet, S. & Achaz, G. (2021) ASAP: assemble species by automatic partitioning. Molecular Ecology Resources, 21 (2), 609–620. https://doi.org/10.1111/1755-0998.13281
  42. Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic biology, 67 (5), 901–904. https://doi.org/10.1093/sysbio/syy032
  43. Ronquist, F., Huelsenbeck, J. & Teslenko, M. (2011) MrBayes version 3.2 Manual: Tutorials and Model Summaries. 172 pp. Available from: https://www.researchgate.net/profile/Fredrik-Ronquist/publication/262493368_Draft_MrBayes_Version_32_Manual_Tutorials_and_Model_Summaries/links/56095a8408ae4d86bb11cf0b/Draft-MrBayes-Version-32-Manual-Tutorials-and-Model-Summaries.pdf (accessed 1 April 2025)
  44. Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19 (12), 1572–1574. https://doi.org/10.1093/bioinformatics/btg180
  45. Sawyer, R. (1972) North American freshwater leeches exclusive of the Piscicolidae, with a key to all species. University of Illinois Press, Urbana, Illinois, 154 pp. https://doi.org/10.5962/bhl.title.53881
  46. Sawyer, R.T. (1986) Leech Biology and Behavior. Clarendon Press, Oxford, 1065 pp.
  47. Siddall, M.E. (2002) Phylogeny of the leech family Erpobdellidae (Hirudinida: Oligochaeta). Invertebrate Systematics, 16, 1–6. https://doi.org/10.1071/IT01011
  48. 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 (1), 23–33. https://doi.org/10.1046/j.1463-6409.2003.00098.x
  49. Siddall, M.E. & Burreson, E.M. (1995) Phylogeny of the Euhirudinea - Independent Evolution of Blood‐Feeding by Leeches. Canadian Journal of Zoology-Revue Canadienne De Zoologie, 73 (6), 1048–1064. https://doi.org/10.1139/z95-125
  50. Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America, 87 (6), 651–701. https://doi.org/10.1093/aesa/87.6.651
  51. Singhal, R. & Davies, R.W. (1985) Descriptions of the reproductive organs of Nephelopsis obscura and Erpobdella punctata (Hirudinoidea: Erpobdellidae). Freshwater Invertebrate Biology, 4 (2), 91–97. https://doi.org/10.2307/1467180
  52. 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
  53. Tamura, K. (1992) Estimation of the number of nucleotide substitutions when there are strong transition‐transversion and G+ C‐content biases. Mol Biol Evol, 9 (4), 678–687.
  54. Tamura, K. & Nei, M. (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10, 512–526.
  55. Tessler, M., de Carle, D., Voiklis, M.L., Gresham, O.A., Neumann, J.S., Cios, S. & Siddall, M.E. (2018a) Worms that suck: Phylogenetic analysis of Hirudinea solidifies the position of Acanthobdellida and necessitates the dissolution of Rhynchobdellida. Molecular Phylogenetics and Evolution, 127, 129–134. https://doi.org/10.1016/j.ympev.2018.05.001
  56. Tessler, M., Siddall, M.E. & Oceguera‐Figueroa, A. (2018b) Leeches from Chiapas, Mexico, with a new species of Erpobdella (Hirudinida: Erpobdellidae). American Museum Novitates, 2018 (3895), 1–15. https://doi.org/10.1206/3895.1
  57. Trajanovski, S., Albrecht, C., Schreiber, K., Schultheiß, R., Stadler, T., Benke, M. & Wilke, T. (2010) Testing the spatial and temporal framework of speciation in an ancient lake species flock: the leech genus Dina (Hirudinea: Erpobdellidae) in Lake Ohrid. Biogeosciences, 7 (11), 3387–3402. https://doi.org/10.5194/bg-7-3387-2010
  58. Trontelj, P. & Sket, B. (2000) Molecular re‐assessment of some phylogenetic, taxonomic and biogeographic relationships between the leech genera Dina and Trocheta (Hirudinea: Erpobdellidae). Hydrobiologia, 438 (1–3), 227–235. https://doi.org/10.1023/A:1004137300113
  59. Uttam, S. & Langer, S. (2021) Distribution and Identification key for species of freshwater leech genus Erpobdella Blainville, 1818 (Hirudinida: Arhynchobdellida: Erpobdelliformes: Erpobdellidae). Eco. Env. & Cons., 27 (4), 1925–1936.
  60. Vilgalys, R. & Hester, M. (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology, 172 (8), 4238–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
  61. Whiting, M.F. (2002) Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zoologica Scripta, 31 (1), 93–104. https://doi.org/10.1046/j.0300-3256.2001.00095.x
  62. Zewayee, F.A. & Ali, L.A. (2024) The first record of Dina prokletijaca (Hirudinida: Erpobdellidae) from Bekhal stream, Erbil, Iraq. Journal of Wildlife and Biodiversity, 8 (1), 54–64.
  63. Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29 (22), 2869–2876. https://doi.org/10.1093/bioinformatics/btt499

How to Cite

Saglam, N., Saunders, R. & Shain, D.H. (2025) Species delimitation recovers undescribed Erpobdellidae (Annelida: Hirudinea) from USA and Türkiye. Zootaxa, 5627 (3), 455–479. https://doi.org/10.11646/zootaxa.5627.3.3