Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
Shopping Cart: ( empty )
You are here: Home > Journals > IS > IS23042
RESEARCH ARTICLE
Contents Vol 37(12)

Lumping three nominal species into one: taxonomic revision of amphibian parasitic leeches of Torix in Far East Asia (Hirudinea: Glossiphoniidae)

Chiaki Kambayashi https://orcid.org/0000-0003-4820-9842 A B * and Takafumi Nakano https://orcid.org/0000-0001-6107-2188 A
+ Author Affiliations
- Author Affiliations

A Department of Zoology, Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan.

B Faculty of Bio-Science, Nagahama Institute of Bio-Science and Technology, Shiga 526-0829, Japan.

* Correspondence to: chkambayashi@gmail.com

Handling Editor: Greg Rouse

Invertebrate Systematics 37(12) 819-833 https://doi.org/10.1071/IS23042
Submitted: 6 August 2023  Accepted: 6 November 2023  Published: 7 December 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing.

Abstract

Although most members of the freshwater leech family Glossiphoniidae have mid-body somites divided into three annuli, the genus Torix Blanchard, 1893 is distinguished by two-annuli somites. Torix has high species richness in Far East Asia, and three nominal species have been recognised in the Japanese Archipelago and adjacent regions that can be distinguished by a combination of both internal and external morphological characteristics. However, recent studies have shown that these diagnostic features are ontogenetically variable and this has resulted in taxonomic confusion among Torix species endemic to the Japanese Archipelago. In this study, we revisit the taxonomic accounts of T. orientalis (Oka, 1925) and T. tagoi (Oka, 1925), in addition to that of the recently redescribed T. tukubana (Oka, 1935) to clarify the diagnostic characteristics for each of the three species. Our morphological and molecular phylogenetic analyses demonstrated that the three Torix species in Japan are indistinguishable. We therefore conclude that these species should be synonymised and treated as a single species. The specific names orientalis and tagoi were simultaneously established under the genus Oligobdella Moore, 1918, therefore we acted as First Reviser and gave precedence to the name O. tagoi, thus the valid name for the Far East Asian Torix species is T. tagoi unless T. orientalis and T. tagoi are treated as distinct species. There are several type localities for T. tagoi and the name-bearing types have been lost, therefore we designate a neotype for this species to obviate zoological and nomenclatural issues.

ZooBank: urn:lsid:zoobank.org:pub:E2DBF999-3B51-456F-AB04-A7D138E0AF2D

Keywords: blood sucking, ectoparasite, Japan, neotypification, redescription, ‘Rhynchobdellida,’ Glossiphoniiformes, synonymisation.

References

Apakupakul K, Siddall ME, Burreson EM (1999) Higher level relationships of leeches (Annelida: Clitellata: Euhirudinea) based on morphology and gene sequences. Molecular Phylogenetics and Evolution 12, 350-359.
| Crossref | Google Scholar | PubMed |

Autrum H (1936) ‘Dr H. G. Bronns Klassen und Ordnungen des Tierreichs. 4. Band: Vermes. III. Abteilung: Annelides. 4. Buch: Hirudineen. Teil 1.’ (Akademische Verlagsgeslellschaft M. B. H.: Leipzig, German Republic) [In German]

Bae YH, Borzée A, Heo J, Jang Y (2018) Rana uenoi (Ueno’s brown frog). Leech parasitism. Herpetological Review 49, 519.
| Google Scholar |

Blanchard R (1893) Torix mirus (novum genus, nova species). Bulletin de la Société Zoologique de France 18, 185-186 [In French].
| Google Scholar |

Blanchard R (1898) Nouveau type d’Hirudinée (Torix mirus). Bulletin Scientifique de la France et la Belgique 28, 339-344 [In French].
| Google Scholar |

Bolotov IN, Klass AL, Kondakov AV, Vikhrev IV, Bespalaya YV, Gofarov MY, Filippov BY, Bogan AE, Lopes-Lima M, Lunn Z, Chan N, Aksenova OV, Dvoryankin GA, Chapurina YE, Kim SK, Kolosova YS, Konopleva ES, Lee JH, Makhrov AA, Palatov DM, Sayenko EM, Spitsyn VM, Sokolova SE, Tomilova AA, Win T, Zubrii NA, Vinarski MV (2019) Freshwater mussels house a diverse mussel-associated leech assemblage. Scientific Reports 9, 16449.
| Crossref | Google Scholar |

Cizauskas CA, Carlson CJ, Burgio KR, Clements CF, Dougherty ER, Harris NC, Phillips AJ (2017) Parasite vulnerability to climate change: an evidence-based functional trait approach. Royal Society Open Science 4, 160535.
| Crossref | Google Scholar | PubMed |

de Carle D, Oceguera-Figueroa A, Tessler M, Siddall ME, Kvist S (2017) Phylogenetic analysis of Placobdella (Hirudinea: Rhynchobdellida: Glossiphoniidae) with consideration of COI variation. Molecular Phylogenetics and Evolution 114, 234-248.
| Crossref | Google Scholar | PubMed |

Eto K, Matsui M, Sugahara T, Tanaka-Ueno T (2012) Highly complex mitochondrial DNA genealogy in an endemic Japanese subterranean breeding brownfrog Rana tagoi (Amphibia, Anura, Ranidae). Zoological Science 29, 662-671.
| Crossref | Google Scholar | PubMed |

Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294-299.
| Google Scholar | PubMed |

Fujisawa T, Barraclough TG (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, 707-724.
| Crossref | Google Scholar | PubMed |

International Commission on Zoological Nomenclature (1999) ‘International Code of Zoological Nomenclature’, 4th edn. (International Trust for Zoological Nomenclature: London, UK)

Jovanović M, Haring E, Sattmann H, Grosser C, Pesic V (2021) DNA barcoding for species delimitation of the freshwater leech genus Glossiphonia from the Western Balkan (Hirudinea, Glossiphoniidae). Biodiversity Data Journal 9, e66347.
| Crossref | Google Scholar | PubMed |

Kambayashi C, Kurabayashi A, Nakano T (2019) Evaluating the ontogenetic external morphology of an ectoparasitic Torix tukubana (Hirudinida: Glossiphoniidae), with records of its new host amphibian species. Parasitology Research 118, 663-666.
| Crossref | Google Scholar | PubMed |

Kambayashi C, Kurabayashi A, Nakano T (2020) Topotype-based redescription of the leech Torix tukubana (Hirudinida: Glossiphoniiformes: Glossiphoniidae). Proceedings of the Biological Society of Washington 133, 59-71.
| Crossref | Google Scholar |

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, 1630-1638.
| Crossref | Google Scholar | PubMed |

Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772-780.
| Crossref | Google Scholar | PubMed |

Kaygorodova IA, Mandzyak NB (2014) Molecular phylogeny of Siberian Glossiphoniidae (Hirudinea). Molecular Biology 48, 523-527.
| Google Scholar | PubMed |

Kaygorodova I, Bolbat N, Bolbat A (2020) Species delimitation through DNA barcoding of freshwater leeches of the Glossiphonia genus (Hirudinea: Glossiphoniidae) from Eastern Siberia, Russia. Journal of Zoological Systematics and Evolutionary Research 58, 1437-1446.
| Crossref | Google Scholar |

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, 1547-1549.
| Crossref | Google Scholar | PubMed |

Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110-1116.
| Crossref | Google Scholar |

Light JE, Siddall ME (1999) Phylogeny of the leech family Glossiphoniidae based on mitochondrial gene sequences and morphological data. The Journal of Parasitology 85, 815-823.
| Google Scholar | PubMed |

Lukin EI (1976) ‘Фауна СССР. Пиявки.’ [‘Fauna USSR. Leeches.’] (Nauka: Leningrad, USSR) [In Russian]

Lukin EI, Epshtein VM (1960) Leeches of the subfamily Toricinae subfam. n. and their geographical distribution. Doklady Akademii Nauk SSSR 134, 478-481 [In Russian].
| Google Scholar |

Mack J, Kvist S (2019) Improved geographic sampling provides further evidence for the separation of Glossiphonia complanata and Glossiphonia elegans (Annelida: Clitellata: Glossiphoniidae). Journal of Natural History 53, 335-350.
| Crossref | Google Scholar |

Medlin L, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71, 491-499.
| Crossref | Google Scholar | PubMed |

Moore JP (1927) The segmentation (metamerism and annulation) of the Hirudinea. In ‘The Fauna of British India, including Ceylon and Burma. Hirudinea’. (Eds WA Harding, JP Moore) pp. 1–12. (Taylor & Francis: London, UK)

Morishima K, Aizawa M (2019) Nuclear microsatellite and mitochondrial DNA analyses reveal the regional genetic structure and phylogeographical history of a sanguivorous land leech, Haemadipsa japonica, in Japan. Ecology and Evolution 9, 5392-5406.
| Crossref | Google Scholar | PubMed |

Morishima K, Fukui E, Aizawa M (2023) Concordant genetic structures of sika deer and Japanese land leeches suggest that the current range expansion of Haemadipsa japonica is dependent on sika deer migration: a case study from Tochigi Prefecture, Japan. Ecological Research 38, 200-210.
| Crossref | Google Scholar |

Nakano T (2010) A new species of the genus Orobdella (Hirudinida: Arhynchobdellida: Gastrostomobdellidae) from Kumamoto, Japan, and a redescription of O. whitmani with the designation of the lectotype. Zoological Science 27, 880-887.
| Crossref | Google Scholar | PubMed |

Nakano T (2012) A new species of Orobdella (Hirudinida, Arhynchobdellida, Gastrostomobdellidae) and redescription of O. kawakatsuorum from Hokkaido, Japan with the phylogenetic position of the new species. ZooKeys 169, 9-30.
| Crossref | Google Scholar |

Nakano T (2016) A new quadrannulate species of Orobdella (Hirudinida, Arhynchobdellida, Orobdellidae) from western Honshu, Japan. ZooKeys 553, 33-51.
| Crossref | Google Scholar | PubMed |

Nakano T, Itoh T (2011) A list of the leech (Clitellata: Hirudinida) collection deposited in the Department of Zoology, the University Museum, the University of Tokyo. The University Museum, The University of Tokyo, Material Reports 90, 85-94.
| Google Scholar |

Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32, 268-274.
| Crossref | Google Scholar | PubMed |

Oceguera-Figueroa A (2012) Molecular phylogeny of the New World bloodfeeding leeches of the genus Haementeria and reconsideration of the biannulate genus Oligobdella. Molecular Phylogenetics and Evolution 62, 508-514.
| Crossref | Google Scholar | PubMed |

Oka A (1925a) Notices sur les Hirudinées d’Extreme Orient, I–IV. Annotationes Zoologicae Japonenses 10, 311-326 [In French].
| Google Scholar |

Oka A (1925b) Notices sur les Hirudinées d’Extreme Orient, V–VII. Annotationes Zoologicae Japonenses 10, 327-335 [In French].
| Google Scholar |

Oka A (1935) Description d’un nouveau genre d’Hirudinée de la famille des Glossiphonides, Oligoclepsis tukuban n. g. n. sp. Proceedings of the Imperial Academy 11, 66-68 [In French].
| Crossref | Google Scholar |

Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21, 1864-1877.
| Crossref | Google Scholar | PubMed |

Puillandre N, Brouillet S, Achaz G (2021) ASAP: assemble species by automatic partitioning. Molecular Ecology Resources 21, 609-620.
| Crossref | Google Scholar | PubMed |

Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901-904.
| Crossref | Google Scholar | PubMed |

Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539-542.
| Crossref | Google Scholar | PubMed |

Sasaki A (2015) 山梨県と静岡県で初記録のタゴビルTorix tagoi (Oka, 1925) [First record of Torix tagoi (Oka, 1925) in Yamanashi Prefecture and Shizuoka Prefecture.]. Natural History of the Tokai District 8, 5-8 [In Japanese].
| Google Scholar |

Sasaki A (2019) 両生類に寄生するTorix属3種の記録 [Three species of the genus Torix parasitic on amphibians.]. Amphibian History 32, 7-9 [In Japanese].
| Google Scholar |

Sawyer RT (1986) ‘Leech Biology and Behaviour.’ (Clarendon Press: Oxford, UK)

Siddall ME, Burreson EM (1998) Phylogeny of leeches (Hirudinea) based on mitochondrial cytochrome c oxidase subunit I. Molecular Phylogenetics and Evolution 9, 156-162.
| Crossref | Google Scholar | PubMed |

Siddall ME, Budinoff RB, Borda E (2005) Phylogenetic evaluation of systematics and biogeography of the leech family Glossiphoniidae. Invertebrate Systematics 19, 105-112.
| Crossref | Google Scholar |

Sket B, Trontelj P (2008) Global diversity of leeches (Hirudinea) in freshwater. Hydrobiologia 595, 129-137.
| Crossref | Google Scholar |

Soós A (1969) Identification key to the leech (Hirudinoidea) genera of the world, with a catalogue of the species. VI. Family: Glossiphoniidae. Acta Zoologica Academiae Scientiarum Hungaricae 15, 397-454.
| Google Scholar |

Tago K (1931) 蠑螈と山椒魚 [‘Imori to Sanshio-uo.’] (Maruzen: Tokyo, Japan) [In Japanese]

White TM, Bruns T, Lee S, Taylor J (1990) Amplification and Direct Sequencing of Fungal Ribosomal RNA for Phylogenetics. In ‘PCR Protocols’. (Eds MA Innis, DH Gelfrand, JJ Sninsky, TJ White) pp. 315–322. (Academic Press: San Diego, CA, USA)

Yang T (1996) 中国动物志. 环节动物门 蛭纲 [‘Fauna Sinica. Annelida Hirudinea.’] (Science Press: Beijing, PR China) [In Chinese]

Yi TL, Pei MT, Xu ZW, Yang DQ (2022) The complete mitochondrial genome of Hemiclepsis yangtzenensis (Clitellata: Glossiphoniidae). Mitochondrial DNA – B. Resources 7, 772-774.
| Crossref | Google Scholar | PubMed |

Yoshida K (2009) 九州未記録種のツクバビル (環形動物門ヒル綱吻蛭目) を天山 (佐賀県唐津市厳木町) で採集 [Occurrence record of Torix tukubana (Annelida: Hirudinea: Rhynchobdellida) collected from Mount Tenzan (Kyuragimachi, Karatsu-shi, Saga Prefecture).]. Saga Nature Study 15, 47 [In Japanese].
| Google Scholar |

Yoshikawa N, Matsui M, Nishikawa K, Kim J-B, Kryukov A (2008) Phylogenetic relationships and biogeography of the Japanese clawed salamander, Onychodactylus japonicus (Amphibia: Caudata: Hynobiidae), and its congener inferred from the mitochondrial cytochrome b gene. Molecular Phylogenetics and Evolution 49, 249-259.
| Crossref | Google Scholar | PubMed |

Yoshinari G, Tamura F, Takano A, Shimura N, Torii H (2022) 奈良県大台ヶ原の底生動物相 [Benthic fauna in Odaigahara, Nara Prefecture.]. Wild Animals of Kii Peninsula 13, 1-13 [In Japanese].
| Google Scholar |

Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 2869-2876.
| Crossref | Google Scholar | PubMed |

Zhu X, Zhao Y, Wei H, Hu N, Hu Q, Li Y (2023) The complete mitochondrial genome of Torix tukubana (Annelida: Hirudinea: Glossiphoniidae). Genes 14, 388.
| Crossref | Google Scholar | PubMed |