Integrative description of two new species of the genus Mesobiotus (Eutardigrada, Macrobiotoidea) from Russia, with an updated phylogeny of the genus

  • Denis V. Tumanov Department of Invertebrate Zoology, Faculty of Biology, Saint Petersburg State University, 199034, Universitetskaya nab. 7/9, Saint Petersburg, Russia https://orcid.org/0000-0002-4190-4175
  • Evgenia D. Androsova Soil Science & Soil Ecology Department, Institute of Earth Sciences, Saint Petersburg State University, 16 Linija, 29, Saint Petersburg, 199178, Russia https://orcid.org/0000-0002-2799-0628
  • Marina D. Gavrilenko Department of Genetics and Biotechnology, Faculty of Biology, Saint Petersburg State University, 199034, Universitetskaya nab. 7/9, Saint Petersburg, Russia https://orcid.org/0009-0009-8847-588X
  • Aidar A. Kalimullin Department of Invertebrate Zoology, Faculty of Biology, Far Eastern Federal University, 10 Ajax Bay, Russky Island, Vladivostok, 690922, Russia https://orcid.org/0009-0006-0380-6183
DOI: https://doi.org/10.5852/ejt.2024.947.2619
Keywords: egg ornamentation, morphology, Mesobiotus mauccii, new species, tardigrades, Macrobiotidae, Far East, North-West

Abstract

In this study, we describe two new species of Mesobiotus based on morphological data collected through light and scanning electron microscopy. Descriptions include DNA sequences of four commonly used molecular markers (18S rDNA, 28S rDNA, ITS-2, and COI). Mesobiotus efa sp. nov. was discovered in North-West Russia and belongs to the group of species with smooth cuticle, harmsworthi-type OCA, typical Mesobiotus claws IV with unindented lunules, and egg chorion with reticulated processes in form of ‘sharp wide cones’ or ‘cones with long slender endings’, egg process bases with well-developed crone of dark thickenings without finger-like projections, and egg shell surface between the processes with ridges without reticulation, areolation or semi-areolation. It can be distinguished from all know species of this group by a unique combination of morphological and morphometric characters. Mesobiotus vulpinus sp. nov. was found in the Russian Far East, and is similar to Mesobiotus mauccii by having an egg chorion with polygonal relief. The new species can be distinguished from M. mauccii by having a narrower buccal tube, by details of oral cavity armature, and by longer egg chorion processes. Furthermore, we provide results of the phylogenetic analyses of the genus Mesobiotus conducted in this study.

References

Abe W. & Takeda M. 2000. Tardigrades from the Imperial Palace, Tokyo. Memoirs of the National Science Museum Tokyo 35: 165–177.

Abe W. & Takeda M. 2005. Semiterrestrial tardigrades from the Tokiwamatsu Imperial Villa, Tokyo, Japan. Memoirs of the National Science Museum Tokyo 39: 503–510.

Beasley C.W. & Miller W.R. 2007. Tardigrada of Xinjiang Uygur Autonomous Region, China. Journal of Limnology 66 (1s): 49–55. https://doi.org/10.4081/jlimnol.2007.s1.49

Beasley C.W. & Miller W.R. 2012. Additional Tardigrada from Hubei Province, China, with the description of Doryphoribius barbarae sp. nov. (Eutardigrada: Parachela: Hypsibiidae). Zootaxa 3170: 55–63. https://doi.org/10.11646/zootaxa.3170.1.5

Bertolani R., Cesari M., Giovannini I., Rebecchi L., Guidetti R., Kaczmarek Ł. & Pilato G. 2023. The Macrobiotus persimilis-polonicus complex (Eutardigrada, Macrobiotidae), another example of problematic species identification, with the description of four new species. Organisms Diversity & Evolution 23: 329–368. https://doi.org/10.1007/s13127-022-00599-z

Biserov V.I. 1991. An annotated list of Tardigrada from European Russia. Zoologische Jahrbücher. Abteilung für Anatomie und Ontogenie der Tiere 118: 193–216.

Biserov V.I. 1996. Tardigrades of the Taimyr Peninsula with description of two new species. Zoological Journal of the Linnean Society 116: 215–237. https://doi.org/10.1111/j.1096-3642.1996.tb02345.x

Biserov V. I. 1997–1998. Tardigrades of the Caucasus with a taxonomic analysis of the genus Ramazzottius (Parachela: Hypsibiidae). Zoologischer Anzeiger 236: 139–159.

Degma P. & Guidetti R. 2023. Actual checklist of Tardigrada species. https://doi.org/10.25431/11380_1178608 [accessed 11 Oct. 2023].

Ganin G.N. 2018. New data on the Drawida (Moniligastridae) tropical earthworms at their northern habitat edge. Vestnik DVO RAN 2018 (4): 49–56 [In Russian.]

Garibian P.G. 2020. Fauna of Cladoceran Crustaceans (Сrustacea: Сladocera) South of the Far East of the Russian Federation and Korean Peninsula. PhD Dissertation, A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences. [In Russian.]

Gouy M., Guindon S. & Gascuel O. 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27 (2): 221–224. https://doi.org/10.1093/molbev/msp259

Guidetti R., Cesari M., Bertolani R., Altiero T. & Rebecchi L. 2019. High diversity in species, reproductive modes and distribution within the Paramacrobiotus richtersi complex (Eutardigrada, Macrobiotidae). Zoological Letters 5: 1. https://doi.org/10.1186/s40851-018-0113-z

Itang L.A.M., Stec D., Mapalo M.A., Mirano-Bascos D. & Michalczyk Ł. 2020. An integrative description of Mesobiotus dilimanensis, a new tardigrade species from the Philippines (Eutardigrada: Macrobiotidae: furciger group). Raffles Bulletin of Zoology 68: 19–31.

Kaczmarek Ł. & Michalczyk Ł. 2017. The Macrobiotus hufelandi group (Tardigrada) revisited. Zootaxa 4363 (1): 101. https://doi.org/10.11646/zootaxa.4363.1.4

Kaczmarek Ł., Gołdyn B., Prokop Z.M. & Michalczyk Ł. 2011. New records of Tardigrada from Bulgaria with the description of Macrobiotus binieki sp. nov. (Eutardigrada: Macrobiotidae) and a key to the species of the harmsworthi group. Zootaxa 2781 (1): 29–39. https://doi.org/10.11646/zootaxa.2781.1.2

Kaczmarek Ł., Cytan J., Zawierucha K., Diduszko D. & Michalczyk Ł. 2014. Tardigrades from Peru (South America), with descriptions of three new species of Parachela. Zootaxa 3790 (2): 357–379. https://doi.org/10.11646/zootaxa.3790.2.5

Kaczmarek Ł., Michalczyk Ł. & McInnes S.J. 2015. Annotated zoogeography of non-marine Tardigrada. Part II: South America. Zootaxa 3923 (1): 1–107. https://doi.org/10.11646/zootaxa.3923.1.1

Kaczmarek Ł., Gawlak M., Bartels P.J., Nelson D.R. & Roszkowska M. 2017. Revision of the genus Paramacrobiotus Guidetti et al., 2009 with the description of a new species, re-descriptions and a key. Annales Zoologici 67 (4): 627–656. https://doi.org/10.3161/00034541ANZ2017.67.4.001

Kaczmarek Ł., Zawierucha K., Buda J., Stec D., Gawlak M., Michalczyk Ł. & Roszkowska M. 2018. An integrative redescription of the nominal taxon for the Mesobiotus harmsworthi group (Tardigrada: Macrobiotidae) leads to descriptions of two new Mesobiotus species from Arctic. PLoS ONE 13 (10): e0204756. https://doi.org/10.1371/journal.pone.0204756

Kaczmarek Ł., Bartylak T., Stec D., Kulpa A., Kepel M., Kepel A. & Roszkowska M. 2020. Revisiting the genus Mesobiotus Vecchi et al., 2016 (Eutardigrada, Macrobiotidae) – remarks, updated dichotomous key and an integrative description of new species from Madagascar. Zoologischer Anzeiger 287: 121–146. https://doi.org/10.1016/j.jcz.2020.05.003

Kaczmarek Ł., Rutkowski T., Zacharyasiewicz M., Surmacki A., Osiejuk T.S. & Hayastha P. 2023. New species of Macrobiotidae (Eutardigrada) from Cameroon (Africa), characteristics of Macrobiotus morpho-groups and a key to the nelsonae group. Annales Zoologici 73: 1–15. https://doi.org/10.3161/00034541ANZ2023.73.1.001

Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., von Haeseler A. & Jermiin L.S. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14: 587–589. https://doi.org/10.1038/nmeth.4285

Katoh K., Misawa K., Kuma K. & Miyata T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30: 3059–3066. https://doi.org/10.1093/nar/gkf436

Kiosya Y., Pogwizd J., Matsko Y., Vecchi M. & Stec D. 2021. Phylogenetic position of two Macrobiotus species with a revisional note on Macrobiotus sottilei Pilato, Kiosya, Lisi & Sabella, 2012 (Tardigrada: Eutardigrada: Macrobiotidae). Zootaxa 4933 (1): 113–135. https://doi.org/10.11646/zootaxa.4933.1.5

Korovchinsky N.M. 2006. The Cladocera (Crustacea: Branchiopoda) as a relict group. Zoological Journal of the Linnean Society 147: 109–124. https://doi.org/10.1111/j.1096-3642.2006.00217.x

Larsson A. 2014. AliView: a fast and lightweight alignment viewer and editor for large data sets. Bioinformatics 30 (22): 3276–3278. https://doi.org/10.1093/bioinformatics/btu531

Likharev I.M. 1953 Features of the distribution of mollusks in Primorsky Krai. Trudy Zoologicheskogo Instituta Academii Nauk SSSR 13: 277–288. [In Russian.]

Mapalo M., Stec D., Mirano-Bascos D.M. & Michalczyk Ł. 2016. Mesobiotus philippinicus sp. nov., the first limnoterrestrial tardigrade from the Philippines. Zootaxa 4126 (3): 411–426. https://doi.org/10.11646/zootaxa.4126.3.6

Mapalo M., Stec D., Mirano-Bascos D. & Michalczyk Ł. 2017. An integrative description of a limnoterrestrial tardigrade from the Philippines, Mesobiotus insanis, new species (Eutardigrada: Macrobiotidae: harmsworthi group). Raffles Bulletin of Zoology 65: 440–454.

Markova T.O., Repsh N.V. & Маslov M.V. 2015. The arealogical analysis of the dipteran fauna (Diptera: Tachinidae, Phasiinae) in the South Primorye. The Bulletin of KrasGAU 2015 (5): 27–30. [In Russian.]

Massa E., Guidetti R., Cesari M., Rebecchi L. & Jönsson K.I. 2021. Tardigrades of Kristianstads Vattenrike Biosphere Reserve with description of four new species from Sweden. Scientific Reports 11: 4861. https://doi.org/10.1038/s41598-021-83627-w

Maucci W. & Durante Pasa M.V. 1980. Tardigradi muscicoli delle Isole Andamane. Bollettino del Museo Civico di Storia Naturale di Verona 7: 281–291.

McInnes S.J. 1991. Notes on tardigrades from the Pyrenees, including one new species. Pedobiologia 35: 11–26. https://doi.org/10.1016/S0031-4056(24)00040-4

Michalczyk Ł. & Kaczmarek Ł. 2003. A description of the new tardigrade Macrobiotus reinhardti (Eutardigrada: Macrobiotidae, harmsworthi group) with some remarks on the oral cavity armature within the genus Macrobiotus Schultze. Zootaxa 331: 1–24. https://doi.org/10.11646/zootaxa.331.1.1

Michalczyk Ł. & Kaczmarek Ł. 2013. The Tardigrada Register: a comprehensive online data repository for tardigrade taxonomy. Journal of Limnology 72 (s1): e22. https://doi.org/10.4081/jlimnol.2013.s1.e22

Miller M.A., Pfeiffer W. & Schwartz T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop (GCE): 1–8. https://doi.org/10.1109/GCE.2010.5676129

Minh B.Q., Schmidt H.A., Chernomor O., Schrempf D., Woodhams M.D., von Haeseler A. & Lanfear R. 2020. IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37: 1530–1534. https://doi.org/10.1093/molbev/msaa015

Morek W., Stec D., Gąsiorek P., Schill R.O., Kaczmarek Ł. & Michalczyk Ł. 2016. An experimental test of eutardigrade preparation methods for light microscopy. Zoological Journal of the Linnean Society 178 (4): 785–793. https://doi.org/10.1111/zoj.12457

Nelson D.R., Bartels P.J. & Guil N. 2018. Tardigrade ecology. In: Schill R.O. (ed.) Water Bears: The Biology of Tardigrades. Zoological Monographs 2: 163–210. Springer Nature Switzerland AG. https://doi.org/10.1007/978-3-319-95702-9_7

Pilato G. 1974. Tre nouve specie di Tardigradi muscicoli di Cina. Animalia 1: 59–68.

Pilato G. 1981. Analisi di nuovi caratteri nello studio degli Eutardigradi. Animalia 8 (1/3): 51–57.

Pilato G. & Binda M.G. 2010. Definition of families, subfamilies, genera and subgenera of the Eutardigrada, and keys to their identification. Zootaxa 2404 (1): 1–54. https://doi.org/10.11646/zootaxa.2404.1.1

Pilato G. & Lisi O. 2006. Macrobiotus rigidus sp. nov., new species of eutardigrade from New Zealand. Zootaxa 1109: 49–55. https://doi.org/10.11646/zootaxa.1109.1.5

Pilato G., Napolitano A. & Manicardi E. 2000. The specific value of Macrobiotus coronatus de Barros, 1942, and description of two new species of the harmsworthi group (Eutardigrada). Bolletino dell’Accademia gioenia di Scienze naturali, Catania 33: 103–120

Pilato G., Sabella G. & Lisi O. 2014. Two new tardigrade species from Sicily. Zootaxa 3754 (2): 173–184. https://doi.org/10.11646/zootaxa.3754.2.6

Pleijel F., Jondelius U., Norlinder E., Nygren A., Oxelman B., Schander C., Sundberg P. & Thollesson M. 2008. Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution 48 (1): 369–371. https://doi.org/10.1016/j.ympev.2008.03.024

Rambaut A., Drummond A.J., Xie D., Baele G. & Suchard M.A. 2018. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67 (5): 901–904. https://doi.org/10.1093/sysbi o/syy032

Ronquist F. & Huelsenbeck J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. https://doi.org/10.1093/bioinformatics/btg180

Roszkowska M., Stec D., Gawlak M. & Kaczmarek Ł. 2018. An integrative description of a new tardigrade species Mesobiotus romani sp. nov (Macrobiotidae; harmsworthi group) from the Ecuadorian Pacific coast. Zootaxa 4450 (5): 550–564. https://doi.org/10.11646/zootaxa.4450.5.2

Short K.A., Sands C.J., McInnes S.J., Pisani D., Stevens M.I. & Convey P. 2022. An ancient, Antarctic-specific species complex: large divergences between multiple Antarctic lineages of the tardigrade genus Mesobiotus. Molecular Phylogenetics and Evolution 170: 107429. https://doi.org/10.1016/j.ympev.2022.107429

Stec D. 2019. Mesobiotus datanlanicus sp. nov., a new tardigrade species (Macrobiotidae: Mesobiotus harmsworthi group) from Lâm Đồng Province in Vietnam. Zootaxa 4679 (1): 164–180. https://doi.org/10.11646/zootaxa.4679.1.10

Stec D. 2021. Integrative descriptions of two new Mesobiotus species (Tardigrada, Eutardigrada, Macrobiotidae) from Vietnam. Diversity 13: 605. https://doi.org/10.3390/d13110605

Stec D. 2022. An integrative description of two new Mesobiotus species (Tardigrada: Eutardigrada: Macrobiotidae) with updated genus phylogeny. Zoological Studies 61: 85. https://doi.org/10.3390/d13110605

Stec D. & Kristensen R.M. 2017. An integrative description of Mesobiotus ethiopicus sp. nov. (Tardigrada: Eutardigrada: Parachela: Macrobiotidae: harmsworthi group) from the Northern Afrotropic region. Turkish Journal of Zoology 41: 800–811. https://doi.org/10.3906/zoo-1701-47

Stec D., Gąsiorek P., Morek W., Kosztyła P., Zawierucha K., Michno K., Kaczmarek Ł., Prokop Z.M. & Michalczyk Ł. 2016. Estimating optimal sample size for tardigrade morphometry. Zoological Journal of the Linnean Society 178 (4): 776–784. https://doi.org/10.1111/zoj.12404

Stec D., Roszkowska M., Kaczmarek Ł. & Michalczyk Ł. 2018. An integrative description of a population of Mesobiotus radiatus (Pilato, Binda and Catanzaro, 1991) from Kenya. Turkish Journal of Zoology 42: 523–540. https://doi.org/10.3906/zoo-1802-43

Stec D., Kristensen R.M. & Michalczyk Ł. 2020a. An integrative description of Minibiotus ioculator sp. nov. from the Republic of South Africa with notes on Minibiotus pentannulatus Londoño et al., 2017 (Tardigrada: Macrobiotidae). Zoologischer Anzeiger 286: 117–134. https://doi.org/10.1016/j.jcz.2020.03.007

Stec D., Krzywański Ł., Zawierucha K. & Michalczyk Ł. 2020b. Untangling systematics of the Paramacrobiotus areolatus species complex by an integrative redescription of the nominal species for the group, with multilocus phylogeny and species delineation in the genus Paramacrobiotus. Zoological Journal of the Linnean Society 188: 694–716. https://doi.org/10.1093/zoolinnean/zlz163

Stec D., Krzywański Ł., Arakawa K. & Michalczyk Ł. 2020c. A new redescription of Richtersius coronifer, supported by transcriptome, provides resources for describing concealed species diversity within the monotypic genus Richtersius (Eutardigrada). Zoological Letters 6: 2. https://doi.org/10.1186/s40851-020-0154-y

Stec D., Vecchi M., Calhim S. & Michalczyk Ł. 2021a. New multilocus phylogeny reorganises the family Macrobiotidae (Eutardigrada) and unveils complex morphological evolution of the Macrobiotus hufelandi group. Molecular Phylogenetics and Evolution 160: 106987. https://doi.org/10.1016/j.ympev.2020.106987

Stec D., Vecchi M., Dudziak M., Bartels P.J., Calhim S. & Michalczyk Ł. 2021b. Integrative taxonomy resolves species identities within the Macrobiotus pallarii complex (Eutardigrada: Macrobiotidae). Zoological Letters 7: 9. https://doi.org/10.1186/s40851-021-00176-w

Stec D., Vončina K., Kristensen R.M. & Michalczyk Ł. 2022. The Macrobiotus ariekammensis species complex provides evidence for parallel evolution of claw elongation in macrobiotid tardigrades. Zoological Journal of the Linnean Society 195: 1067–1099. https://doi.org/10.1093/zoolinnean/zlab101

Tamura K., Stecher G. & Kumar S. 2021. MEGA11: Molecular Evolutionary Genetics Analysis version 11. Molecular Biology and Evolution 38: 3022–3027. https://doi.org/10.1093/molbev/msab120

Tumanov D.V. 2018a. Hypsibius vaskelae, a new species of Tardigrada (Eutardigrada, Hypsibiidae) from Russia. Zootaxa 4399 (3): 434. https://doi.org/10.11646/zootaxa.4399.3.12

Tumanov D.V. 2018b. Mesobiotus nikolaevae sp. n. (Eutardigrada: Macrobiotidae), a new species of Tardigrada from Croatia. Invertebrate Zoology 15 (4): 402–419. https://doi.org/10.15298/invertzool.15.4.08

Tumanov D.V. 2020a. Integrative description of Mesobiotus anastasiae sp. nov. (Eutardigrada, Macrobiotoidea) and first record of Lobohalacarus (Chelicerata, Trombidiformes) from the Republic of South Africa. European Journal of Taxonomy 726: 102–132. https://doi.org/10.5852/ejt.2020.726.1179

Tumanov D.V. 2020b. Integrative redescription of Hypsibius pallidoides Pilato et al., 2011 (Eutardigrada: Hypsibioidea) with the erection of a new genus and discussion on the phylogeny of Hypsibiidae. European Journal of Taxonomy 681: 1–37. https://doi.org/10.5852/ejt.2020.681

Tumanov D.V. & Pilato G. 2019. A new species of Eutardigrade (Macrobiotidae) from New Zealand. Zootaxa 4603 (3): 537–548. https://doi.org/10.11646/zootaxa.4603.3.6

Tumanov D.V., Androsova E.D., Avdeeva G.S. & Leontev A.A. 2022. First faunistic investigation of semiterrestrial tardigrade fauna of North-West Russia using the method of DNA barcoding. Invertebrate Zoology 19 (4): 452–474. https://doi.org/10.15298/invertzool.19.4.08

Utsugi K. 1988. Tardigrades in Hokkaido area. Zoological Science 5: 1335.

Vecchi M., Cesari M., Bertolani R., Jönsson K.I., Rebecchi L. & Guidetti R. 2016. Integrative systematic studies on tardigrades from Antarctica identify new genera and new species within Macrobiotoidea and Echiniscoidea. Invertebrate Systematics 30 (4): 303–322. https://doi.org/10.1071/IS15033

Vecchi M., McDaniel J.L., Chartrain J., Vuori T., Walsh E.J. & Calhim S. 2023. Morphology, phylogenetic position, and mating behaviour of a new Mesobiotus (Tardigrada) species from a rock pool in the Socorro Box Canyon (New Mexico, USA). The European Zoological Journal 90 (2): 708–725. https://doi.org/10.1080/24750263.2023.2263033

Vecchi M., Stec D., Rebecchi L., Michalczyk Ł. & Calhim S. 2024. Ecology explains anhydrobiotic performance across tardigrades, but the shared evolutionary history matters more. Journal of Animal Ecology 93: 307–318. https://doi.org/10.1111/1365-2656.14031

Published
2024-07-30
How to Cite
Tumanov, D. V., Androsova, E. D., Gavrilenko, M. D., & Kalimullin, A. A. (2024). Integrative description of two new species of the genus Mesobiotus (Eutardigrada, Macrobiotoidea) from Russia, with an updated phylogeny of the genus. European Journal of Taxonomy, 947(1), 20–52. https://doi.org/10.5852/ejt.2024.947.2619
Issue
Vol. 947 (2024)
Section
Research article

Copyright (c) 2024 Denis V. Tumanov, Evgenia D. Androsova, Marina D. Gavrilenko, Aidar A. Kalimullin

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Creative Commons Copyright Notices

Authors who publish with this journal agree to the following terms:

  1. Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License (CC BY 4.0) that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
  2. Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
  3. Authors are NOT ALLOWED TO post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to taxonomic issues.