Abstract
In this paper, three new enchytraeid species (Enchytraeidae, Clitellata) are described from different mountains of Korea: Cognettia koreana sp. n., Henlea bidiverticulata sp. n. and Mesenchytraeus longidiverticulatus sp. n. Validity of these new species was confirmed by comparative morphological and molecular taxonomic analyses (based on ITS, CO1 and H3 sequences). In addition, ten enchytraeid species never recorded before from Korea were found in the studied soil samples: Bryodrilus diverticulatus Černosvitov, 1929, Cernosvitoviella atrata Bretscher, 1903, Cernosvitoviella minor Dózsa-Farkas, 1990, Cognettia lapponica Nurminen, 1965, Cognettia varisetosa (Martinsson, Rota & Erséus, 2015), Fridericia cf. sohlenii Rota, Healy & Erséus, 1998, Henlea nasuta Eisen, 1878, Marionina clavata Nielsen & Christensen, 1961, Marionina communis Nielsen & Christensen, 1959, Marionina seminuda Xie & Rota, 2001. Morphological observations and new reference DNA sequences are also provided for the above-mentioned species.
References
Altman, L.C. (1936) Oligochaeta of Washington. University of Washington Publications in Biology, 4, 1–137.
Bell, A.W. (1942) Some new enchytraeid worms (Oligochaeta) from North America. Transactions of the American Microscopical Society, 61, 404–429.
https://doi.org/10.2307/3222906
Bretscher, K. (1903) Beobachtungen über die Oligochaeten der Schweiz VII. Folge. Revue Suisse de Zoologie, 11, 1–21.
https://doi.org/10.5962/bhl.part.75163
Cech, G., Boros, G. & Dózsa-Farkas, K. (2012) Revision of Bryodrilus glandulosus (Dózsa-Farkas, 1990) and Mesenchytraeus kuehnelti Dózsa-Farkas, 1991 (Oligochaeta: Enchytraeidae) using morphological and molecular data. Zoologischer Anzeiger, 251, 253–262.
https://doi.org/10.1016/j.jcz.2011.09.005
Černosvitov, L. (1928) Die Oligochaetenfauna der Karpathen. Zoologische Jahrbücher. Abteilung für Systematik, Geographie und Biologie der Tiere. Jena, 55, 1–2.
Černosvitov, L. (1929) Communication preliminaire sur les Oligochètes récoltés par M. P. Remy pendant la croisière arctique effectuée par le “Pourquoi-Pas?” en 1926 sous la sirection du Dr. J.-B. Charcot. Bulletin du Muséum National d’Histoire Naturelle, Paris, 2 (1), 144–149.
Černosvitov, L. (1937) System der Enchytraeiden. Bulletin de l’Association Russe pour les Recherches Scientifiques a Prague, 5 (34), 263–295.
Chalupský, J. (1992) Terrestrial Enchytraeidae (Oligochaeta) and Parergodrilidae (Polychaeta) from Sweden, with description of a new enchytraeid species. Zoologica Scripta, 21, 133–150.
https://doi.org/10.1111/j.1463-6409.1992.tb00316.x
Chen, J., Jiang, W. & Xie, Z. (2016) First records of Enchytraeidae (Annelida, Clitellata) from the Three Parallel Rivers region. Zootaxa, 4093 (2), 275–284.
https://doi.org/10.11646/zootaxa.4093.2.8
Christensen, B. & Dózsa-Farkas, K. (1999) The enchytraeid fauna of the Palearctic tundra (Oligochaeta, Enchytraeidae). Biologiske Skrifter, The Royal Danish Academy of Sciences and Letters, 52, 1–37.
Christensen, B. & Dózsa-Farkas, K. (2006) Invasion of terrestrial enchytraeids into two glacial tundras: North-eastern Greenland and the Arctic Achipelago of Canada (Enchytraeidae, Oligochaeta). Polar Biology, 29, 454–466.
https://doi.org/10.1007/s00300-005-0076-3
Christensen, B. & Glenner, H. (2010) Molecular phylogeny of Enchytraeidae (Oligochaeta) indicates separate invasions of the terrestrial environment. Journal of Zoological Systematics and Evolutionary Research, 48, 208–212.
https://doi.org/10.1111/j.1439-0469.2009.00558.x
Christensen, B. & Dózsa-Farkas, K. (2012) A new genus Globulidrilus and three new enchytraeid species (Oligochaeta: Enchytraeidae) from Seoraksan National Park (Korea). Journal of Natural History, 46, 2769–2785.
https://doi.org/10.1080/00222933.2012.737038
Colgan, D.J., McLauchlan, A.A., Wilson, G.D.F., Livingston, S.P., Edgecombe, G.D., Macaranas, J., Cassis, G. & Gray, M.R. (1998) Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Australian Journal of Zoology, 46, 419–437.
https://doi.org/10.1071/ZO98048
Dózsa-Farkas, K. (1970) The description of three new species and some data to the enchytraeid fauna of the Baradla Cave, Hungary. Opuscula Zoologica Budapest, 10, 241–251.
Dózsa-Farkas, K. (1989) Neue Enchytraeiden-Arten (Oligochaeta) aus Ekuador. Acta Zoologica Hungarica, 35, 191–203.
Dózsa-Farkas, K. (1990) New enchytraeid species from sphagnum-bogs in Hungary (Oligochaeta: Enchytraeidae). Acta Zoologica Hungarica, 36, 265–274.
Dózsa-Farkas, K. & Hong, Y. (2010) Three new Hemienchytraeus species (Enchytraeidae, Oligochaeta, Annelida) from Korea, with first records of other enchytraeids and terrestrial polychaetes (Annelida). Zootaxa, 2406 (1), 29–56.
https://doi.org/10.11646/zootaxa.2406.1.2
Dózsa-Farkas, K., Porco, D. & Boros, G. (2012) Are Bryodrilus parvus Nurminen, 1970 and Bryodrilus librus (Nielsen and Christensen, 1959) really different species? A revision based on DNA barcodes and morphological data. Zootaxa, 3276 (1), 38–50.
https://doi.org/10.11646/zootaxa.3276.1.2
Dózsa-Farkas, K. & Felföldi, T. (2015) Unexpected occurrence of Hemifridericia bivesiculata Christensen & Dózsa-Farkas, 2006 in Hungary, a species presumed to be endemic to Devon Island, Canada, and its comparative analysis with H. parva Nielsen & Christensen, 1959 (Enchytraeidae, Oligochaeta). Zootaxa, 3914 (2), 185–194. https://doi.org/10.11646/zootaxa.3914.2.8
Dózsa-Farkas, K., Felföldi, T. & Hong, Y. (2015) New enchytraeid species (Enchytraeidae, Oligochaeta) from Korea. Zootaxa, 4006 (1), 171–197.
https://doi.org/10.11646/zootaxa.4006.1.9
Dózsa-Farkas, K. & Felföldi, T. (2017) Comparative morphological and molecular taxonomic study of six Achaeta species (Clitellata: Enchytraeidae) with the description of a new Achaeta species from Kőszeg Mountains, Hungary. Zootaxa, 4273 (2), 177–194.
https://doi.org/10.11646/zootaxa.4273.2.2
Dózsa-Farkas, K., Csitári, B. & Felföldi, T. (2017) A new Cernosvitoviella species (Clitellata: Enchytraeidae) and its comparison with other Cernosvitoviella species from Sphagnum mires in Hungary. Zootaxa, 4254 (3), 322–338.
https://doi.org/10.11646/zootaxa.4254.3.2
Dózsa-Farkas, K., Felföldi, T., Nagy, H. & Hong, Y. (2018) New enchytraeid species from Mount Hallasan (Jeju Island, Korea) (Enchytraeidae, Oligochaeta). Zootaxa, 4496 (1), 337–381.
https://doi.org/10.11646/zootaxa.4496.1.27
Dózsa-Farkas, K. (2019) Enchytraeids of Hungary (Annelida: Clitellata: Enchytraeidae). Pedozoologica Hungarica. Vol. 7. Eötvös University Press, Budapest, 226 pp.
Dózsa-Farkas, K., Felföldi, T., Nagy, H. & Hong, Y. (2019a) Two new enchytraeid species (Annelida, Enchytraeidae) from Jeju Island, Korea. ZooKeys, 824, 87–108.
https://doi.org/10.3897/zookeys.824.25544
Dózsa-Farkas, K., Nagy, H., Felföldi, T. & Hong, Y. (2019b) Decimodrilus, a new enchytraeid genus from Korea (Annelida, Clitellata, Enchytraeidae). Zootaxa, 4661 (2), 385–399.
https://doi.org/10.11646/zootaxa.4661.2.7
Dózsa-Farkas, K., Nagy, H. & Felfödi, T. (2019c) Two new species of Fridericia (Annelida: Enchytraeidae) from Hungarian caves. European Journal of Taxonomy, 553, 1–18.
https://doi.org/10.5852/ejt.2019.553
d’Udekem, J. (1854) Description d’une nouvelle espèce d’Enchytraeus. Bulletins de l’Académie Royale des Sciences de Belgique, 21, 853–865.
Eisen, G. (1878) Redogörelse för Oligochaeter samlade under de Svenska expeditionerna till Arktiska trakter. Öfversigt af Kongliga Vetenskaps-Akademiens Förhandlingar, 3, 63–79.
Eisen, G. (1904) Enchytraeidae of the West Coast of North America. Harriman Alaska Series, New York, 12, 1–126.
https://doi.org/10.5962/bhl.title.11673
Emery, C. (1898) Diagnosi di un nuovo genere e nuova specie di Annellidi della famiglia degli Enchytraeidae. Mesenchytraeus solifugus. R. Accademia nazionale dei Lincei. Classe di scienze fisishe matematiche e naturali (5). Rendiconti, 7, 110–111.
Erséus, C. (1990) Marine Oligochaeta of Hong Kong. In: Morton, B. (Ed.), The Marine Flora and Fauna of Hong Kong and Southern China II. Vol. 1. Introduction and taxonomy: Hong Kong University Press, Hong Kong, pp. 260–334.
Erséus, C., Rota, E., Matamoros, L. & De Wit, P. (2010) Molecular phylogeny of Enchytraeidae (Annelida, Clitellata). Molecular Phylogenetics and Evolution, 57 (2), 849–858.
https://doi.org/10.1016/j.ympev.2010.07.005
Erséus, C., Rota, E., Timm, T., Grimm, R., Healy, B. & Lundberg, S. (2005) Riverine and riparian clitellates of three drainages in southern Sweden. Annales de Limnologie, Toulouse, 41, 183–194.
https://doi.org/10.1051/limn:20054130183
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.
Friend, H. (1911) New British Henleas. The Zoologist, Series 4 15, 464–468.
Friend, H. (1913) British enchytraeids. V. Species new to science. Journal of the Royal Microscopical Society, 1913, 255271.
Graefe, U., Dózsa-Farkas, K. & Christensen, B. (2005) Achaeta unibulba sp. n., a widespread European species (Oligochaeta, Enchytraeidae). Proceedings of the Estonian Academy of Sciences: Biology, Ecology, 54, 271–278.
Healy, B. (1975) A description of five new species of Enchytraeidae (Oligochaeta) from Ireland. Zoological Journal of the Linnean Society, 56, 315–326.
https://doi.org/10.1111/j.1096-3642.1975.tb00273.x
Healy, B. (1996) Records of Enchytraeidae (Annelida: Oligochaeta) from west Florida. 1. Mesenchytraeus, Cognettia, Bryodrilus, Hemienchytraeus, Henlea and Buchholzia. Proceedings of the Biological Society of Washington, 109, 118–137.
Healy, B. & Coates, K.A. (1997) Enchytraeids (Oligochaeta: Annelida) of the mid and upper intertidal of Darwin Harbour, Northern Territory, Australia. In: Hanley, J.R., Caswell, G., Megirian, D. & Larsen, H.K. (Eds.), Proceedings of the Sixth International Marine Biological Workshop. The Marine Flora and Fauna of Darwin Harbour, Northern Territory, Australia. Museums and Art Galleries of the Northern Territory and the Australian Marine Sciences Association, Darwin, pp.81–97.
Healy, B & Timm, T. (2000) Mesenchytraeus kuril, a new species of Enchytraeidae (Annelida: Oligochaeta) from Kamčatka, Russian Far East. Species Diversity, 5, 177–182.
https://doi.org/10.12782/specdiv.5.177
Hong, Y. & Dózsa-Farkas, K. (2018) New descriptions of enchytraeid species (Clitellata: Enchytraeidae) from Korea. Journal of Species Research, 7 (1), 80–91.
https://doi.org/10.12651/JSR.2018.7.1.080
Issel, R. (1905) Oligocheti inferiori della fauna italiana. I. Enchitreidi di Val Pellice. Zoologische Jahrbücher. Abteilung für Anatomie und Ontogenie der Tiere, Jena, 22, 451– 476.
Kane, R.A. & Rollinson, D. (1994) Repetitive sequences in the ribosomal DNA internal transcribed spacer of Schistosoma haematobium, Schistosoma intercalatum and Schistosoma mattheii. Molecular and Biochemical Parasitology, 63, 153–156. https://doi.org/10.1016/0166-6851(94)90018-3
Klinth, M.J., Martinsson, S. & Erséus, C. (2017) Phylogeny and species delimitation of North European Lumbricillus (Clitellata, Enchytraeidae). Zoologica Scripta, 46, 96–110.
https://doi.org/10.1111/zsc.12187
Knöllner, F. H. (1935) Ökologische und systematische Untersuchungen über litorale und marine Oligochäten der Kieler Bucht. Zoologische Jahrbücher. Abteilung für Systematik, Geographie und Biologie der Tiere, Jena, 66, 425–512.
Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874.
https://doi.org/10.1093/molbev/msw054
Lang, S.A., Saglam, N., Kawash, J. & Shain, D.H. (2017) Punctuated invasion of water, ice, snow and terrestrial ecozones by segmented worms (Oligochaeta: Enchytraeidae: Mesenchytraeus). Proceedings of the Royal Society B, 284, 20171081.
https://doi.org/10.1098/rspb.2017.1081
Leray, M., Knowlton, N., Ho, S.L., Nguyen, B.N. & Machida, R.J. (2019) GenBank is a reliable resource for 21st century biodiversity research. Proceedings of the National Academy of Sciences of the U.S.A., 116 (45), 22651–22656.
https://doi.org/10.1073/pnas.1911714116
Leuckart, R. (1847) s.n. In: Frey, H. & Leuckart, R. (1847) Beiträge zur Kenntnis der wirbellosen Tiere mit besonderer Berücksichtigung der Fauna des Nord-deutschen Meeres, Braunschweig, 4, pp. 1–170.
Levinsen, G.M.R. (1884) Systematisk-geografisk Oversigt over de nordiske Annulata, Gephyrea, Chaetognathi og Balanoglossi. II. Videnskabelige Meddelelser fra den Naturhistoriske Forening i Kjøbenhavn for Aaret, 1883, 92–350.
https://doi.org/10.5962/bhl.title.16117
Martinsson, S. & Erséus, C. (2014) Cryptic diversity in the well-studied terrestrial worm Cognettia sphagnetorum (Clitellata: Enchytraeidae). Pedobiologia, 57 (1), 27–35.
https://doi.org/10.1016/j.pedobi.2013.09.006
Martinsson, S., Rota, E. & Erséus, C. (2015a) Revision of Cognettia (Clitellata, Enchytraeidae): re-establishment of Chamaedrilus and description of cryptic species in the sphagnetorum complex. Systematics and Biodiversity, 13 (3), 257–277. https://doi.org/10.1080/14772000.2014.986555
Martinsson, S., Rota, E. & Erséus, C. (2015b) On the identity of Chamaedrilus glandulosus (Michaelsen, 1888) (Clitellata, Enchytraeidae), with the description of a new species. Zookeys, 501, 1–14.
https://doi.org/10.3897/zookeys.501.9279
Martinsson, S., Dózsa-Farkas, K., Rota, E. & Erséus, C. (2017) Placing the forgotten: on the positions of Euenchytraeus and Chamaedrilus in an updated enchytraeid phylogeny (Clitellata: Enchytraeidae). Invertebrate Systematics, 31, 85–90. https://doi.org/10.1071/IS16042
Martinsson, S. (2019) A morphology-based identification key to the Cognettia species of the world (Clitellata: Enchytraeidae). Soil Organisms, 91 (2), 37–43.
https://doi.org/10.25674/so91103
Matamoros, L., Rota, E. & Erséus, C. (2012) Cryptic diversity among the achaetous Marionina (Annelida, Clitellata, Enchytraeidae). Systematics and Biodiversity, 10, 509–525.
https://doi.org/10.1080/14772000.2012.723640
Michaelsen, W. (1888) Beiträge zur Kenntnis der deutschen Enchyträiden-fauna. Archiv für Mikroskopische Anatomie, 31, 483–498.
https://doi.org/10.1007/BF02955717
Michaelsen, W. (1889) Oligochaeten des Naturhistorischen Museums in Hamburg. I. Jahrbuch der Hamburgischen Wissenschaftlichen Anstalten, 6, 1–17.
Nagy, H., Dózsa-Farkas, K., Hong, Y. & Felföldi, T. (2020) Extending the geographic distribution of Bryodrilus ehlersi (annelida, Enchytraeidae): morphological and molecular comparison of Korean and European specimens. Acta Zoologica Academiae Scientiarum Hungaricae, 66 (4), 345–360.
https://doi.org/10.17109/AZH.66.4.345.2020
Nielsen, C.O. & Christensen, B. (1959) The Enchytraeidae. Critical revision and taxonomy of European species (studies on Enchytraeidae VII). Natura Jutlandica, 8–9, 1–160.
Nielsen, C.O. & Christensen, B. (1961) The Enchytraeidae. Critical revision and taxonomy of European species. Supplement 1. Natura Jutlandica, 10, 1–23.
Nurminen, M. (1965) Enchytraeids (Oligochaeta) from northern Norway and western Lappland. Annales Zoologici Fennici, 2, 11–15.
Nurminen, M. (1970) Records of Enchytraeidae (Oligochaeta) from the west coast of Greenland. Annales Zoologici Fennici, 7, 199–209.
O’Connor, F.B. (1962) The extraction of Enchytraeidae from soil. In: Murphy, P.W. (Ed.), Progress in soil zoology, London, pp. 279–285.
Piper, S.R., MacLean, S.F. & Christensen, B. (1982) Enchytraeidae (Oligochaeta) from taiga and tundra habitats of northeastern U.S.S.R. Canadian Journal of Zoology, 60, 2594–2609.
https://doi.org/10.1139/z82-334
Righi, G. & Kanner, E. (1979) Marine Oligochaeta (Tubificidae and Enchytraeidae) from the Caribbean Sea. Studies of the Fauna of Curaçao and other Caribbean Islands, 58, 44–68.
Rota, E. (1995) Italian Enchytraeidae (Oligochaeta). I. Bollettino di Zoologia, 62, 183–231.
https://doi.org/10.1080/11250009509356067
Rota, E., Healy, B. & Erséus, C. (1998) Biogeography and taxonomy of terrestrial Enchytraeidae (Oligochaeta) in Northern Sweden, with comparative remarks on the genus Henlea. Zoologischer Anzeiger, 237, 155–169.
Rota, E. & Brinkhurst, R.O. (2000) Mesenchytraeus antaeus, a new giant enchytraeid (Annelida, Clitellata) from the temperate rainforest of British Columbia, Canada, with a revised diagnosis of the genus Mesenchytraeus. The Journal of Zoology, London, 252, 27–40.
https://doi.org/10.1111/j.1469-7998.2000.tb00817.x
Rota, E. & Manconi, R. (2004) Taxonomy and ecology of sponge-associate Marionina spp. (Clitellata: Enchytraeidae) from the Horomatangi Geothermal System of Lake Taupo, New Zeeland. International Review of Hydrobiology, 89 (1), 58–67.
https://doi.org/10.1002/iroh.200310695
Rota, E., Martinsson, S. & Erséus, C. (2018) Two new bioluminescent Henlea from Siberia and lack of molecular support for Hepatogaster (Annelida, Clitellata, Enchytraeidae), Organisms Diversity & Evolution, 18 (3), 291–312.
https://doi.org/10.1007/s13127-018-0374-6
Schmelz, R.M. (2003) Taxonomy of Fridericia (Oligochaeta, Enchytraeidae). Revision of species with morphological and biochemical methods. Abhandlungen des Naturwissenschaftlichen Vereins in Hamburg, Neue Folge, 38, 1–415.
Schmelz, R.M. & Collado, R. (2010) A guide to European terrestrial and freshwater species of Enchytraeidae (Oligochaeta). Soil Organisms, 82 (1), 1–176.
Schmelz, R.M., Jocque, M. & Collado, R. (2015) Microdrile Oligochaeta in bromeliad pools of a Honduran cloud forest. Zootaxa, 3947 (4), 508–526.
https://doi.org/10.11646/zootaxa.3947.4.3
Schmelz, R.M., Beylich, A., Boros, G., Dózsa-Farkas, K., Graefe, U., Hong, Y., Römbke, J., Schlaghamerský, J. & Martinsson, S. (2017) How to deal with cryptic species in Enchytraeidae, with recommendations on taxonomical descriptions. Opuscula Zoologica Budapest, 48 (S2), 45–51.
https://doi.org/10.18348/opzool.2017.S2.45
Shelton, A.O., O’Donnell, J.L., Samhouri, J.F., Lowell, N., Williams, G.D. & Kelly, R.P. (2016) A framework for inferring biological communities from environmental DNA. Ecological Applications, 26 (6), 1645-1659.
https://doi.org/10.1890/15-1733.1.
Shen, Q., Chen, J. & Xie, Z. (2012) Mesenchytraeus monodiverticulatus sp. nov. (Annelida; Clitellata: Enchytraeidae) from Changbai Mountain, with a key to Mesenchytraeus with enlarged chaetae. Proceedings of the Biological Society of Washington, 125 (3), 215–227.
https://doi.org/10.2988/12-08.1
Southern, R. (1909) Contributions towards a monograph of the British and Irish Oligochaeta. Proceedings of the Royal Irish Academy, 27 (B), 119–182.
Timm, T. & Popchenko, V. (1978) The aquatic Oligochaeta from lakes of the Murmansk Region. Hydrobiological Researches, Institute of Zoology and Botany of the Estonian Academy of Sciences, 7, 79–111.
Ude, H. (1892) Ein neues Enchytraeiden-Genus. Zoologischer Anzeiger, 401, 344–345.
Vejdovský, F. (1878) Zur Anatomie und Systematik der Enchytraeiden. Sitzungsberichte der Königlich Böhmischen Gesellschaft der Wissenschaften, 1877, 294–304.
Welch, P.S. (1914) Studies on the Enchytraeidae of North America. Bulletin of the Illinois State Laboratory of Natural History, Urbana, 10, 123–211.
https://doi.org/10.21900/j.inhs.v10.373
Welch, P.S. (1916) Snow-field and glacier Oligochaeta from Mt. Rainier, Washington. Transactions of the American Microscopical Society, 35, 85–124.
https://doi.org/10.2307/3221561
Welch, P.S. (1919) Further studies on North American Mesenchytraeids (Oligochaeta). Transactions of the American Microscopical Society, 38, 175–188.
https://doi.org/10.2307/3221532
Xie, Z. & Rota, E. (2001) Four new terrestrial species of Marionina (Clitellata, Enchytraeidae) from China and re-examination of M. hoffbaueri Möller. Journal of Natural History, 35, 1417–1431.
https://doi.org/10.1080/002229301317067610