Abstract
Marine tardigrades in the Antarctic and sub-Antarctic regions are poorly understood. During the 59th Japan Antarctic Research Expedition, a sediment sample was collected from Lützow-Holm Bay, East Antarctica. The sediment sample yielded three species of marine tardigrades belonging to the family Styraconyxidae Kristensen & Renaud-Mornant, 1983: Angursa antarctica Villora-Moreno, 1998, Styraconyx cf. qivitoq Kristensen & Higgins, 1984, and S. takeshii sp. nov. The new species resembles S. nanoqsunguak Kristensen & Higgins, 1984 by the overall morphology, but the new species has thick seminal receptacle ducts that do not terminate in typical, swelled vesicles, in contrast to S. nanoqsunguak’s narrow seminal receptacle ducts that terminate in small vesicles. The presence of the undivided mouth papilla and the larger body further differentiates the new species from S. nanoqsunguak. We also report a young adult female with a gonopore, but lacking seminal receptacles in the new species. As well as morphological information, we provided the sequences of the new species’ nuclear 28S rRNA and mitochondrial cytochrome c oxidase subunit I fragments. Using the former molecular data, phylogenetic analyses of Styraconyxidae were conducted and polyphyly of Styraconyx was suggested. The biogeography of marine tardigrades in the Antarctic and sub-Antarctic regions are also discussed.
Similar content being viewed by others
References
Bartels PJ, Apodaca JJ, Mora C, Nelson DR (2016) A global biodiversity estimate of a poorly known taxon: phylum Tardigrada. Zool J Linn Soc 178:730–736. https://doi.org/10.1111/zoj.12441
Bellido A, Bertrand M (1981) Echiniscoides travei n. sp., un tardigrade marin des îles Kerguelen (Heterotardigrada). Bull Mus natn Hist Nat Paris 4e Sér 3 Sect A:789–798
Brannock PM, Learman DR, Mahon AR, Santos SR, Halanych KM (2018) Meiobenthic community composition and biodiversity along a 5500 km transect of Western Antarctica: a metabarcoding analysis. Mar Ecol Prog Ser 603:47–60. https://doi.org/10.3354/meps12717
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334
Cesari M, McInnes SJ, Bertolani R, Rebecchi L, Guidetti R (2016) Genetic diversity and biogeography of the south polar water bear Acutuncus antarcticus (Eutardigrada : Hypsibiidae)—evidence that it is a truly pan-Antarctic species. Invertebr Syst 30:635–649. https://doi.org/10.1071/IS15045
Convey P (1997) How are the life history strategies of Antarctic terrestrial invertebrates influenced by extreme environmental conditions? J Therm Biol 22:429–440. https://doi.org/10.1016/S0306-4565(97)00062-4
Convey P, McInnes SJ (2005) Exceptional tardigrade-dominated ecosystems in Ellsworth Land, Antarctica. Ecology 86:519–527. https://doi.org/10.1890/04-0684
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
Degma P, Guidetti R (2007) Notes to the current checklist of Tardigrada. Zootaxa 1579:41–53. https://doi.org/10.11646/zootaxa.1579.1.2
Degma P, Bertolani R, Guidetti R (2009–2018) Actual checklist of Tardigrada species (34th edn: 30-06-2018). https://www.tardigrada.modena.unimo.it/miscellanea/Actual%20checklist%20of%20Tardigrada.pdf. Accessed 27 June 2019
De Zio Grimaldi S, Gallo D’Addabbo M, Pietanza R (2000) Two new sub-Antarctic Echiniscoididae from Marion Island (Heterotardigrada, Echiniscoidea). Ital J Zool 67:221–228. https://doi.org/10.1080/11250000009356315
Fabiano M, Danovaro R (1999) Meiofauna distribution and mesoscale variability in two sites of the Ross Sea (Antarctica) with contrasting food supply. Polar Biol 22:115–123. https://doi.org/10.1007/s003000050398
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. Mol Mar Biol Biotechnol 3:294–299
Fonseca VG, Sinniger F, Gaspar JM, Quince C, Creer S, Power DM, Peck LS, Clark MS (2017) Revealing higher than expected meiofaunal diversity in Antarctic sediments: a metabarcoding approach. Sci Rep 7:6094. https://doi.org/10.1038/s41598-017-06687-x
Fujimoto S, Hansen JG (2019) Revision of Angursa (Arthrotardigrada: Styraconyxidae) with the description of a new species from Japan. Eur J Taxon 510:1–19. https://doi.org/10.5852/ejt.2019.510
Fujimoto S, Jimi N (2020) A new marine tardigrade genus and species (Arthrotardigrada, Styraconyxidae) with unique pockets on the legs. Zoosyst Evol 96:115–122. https://doi.org/10.3897/zse.96.49676
Fujimoto S, Jørgensen A, Hansen JG (2017) A molecular approach to arthrotardigrade phylogeny (Heterotardigrada, Tardigrada). Zool Scr 46:496–505. https://doi.org/10.1111/zsc.12221
Giere O (2009) Meiobenthology: the microscopic motile fauna of aquatic sediments. Springer, Berlin
Guidetti R, Bertolani R (2005) Tardigrade taxonomy: an updated checklist of the taxa and a list of characters for their identification. Zootaxa 845:1–46. https://doi.org/10.11646/zootaxa.845.1.1
Guidetti R, Rebecchi L, Cesari M, McInnes SJ (2014) Mopsechiniscus franciscae, a new species of a rare genus of Tardigrada from continental Antarctica. Polar Biol 37:1221–1233. https://doi.org/10.1007/s00300-014-1514-x
Guidetti R, McInnes SJ, Cesari M, Rebecchi L, Rota-Stabelli O (2017) Evolutionary scenarios for the origin of an Antarctic tardigrade species based on molecular clock analyses and biogeographic data. Contrib Zool 86:97–110. https://www.ctoz.nl/vol86/nr02/a01
Guidetti R, Massa E, Bertolani R, Rebecchi L, Cesari M (2019) Increasing knowledge of Antarctic biodiversity: new endemic taxa of tardigrades (Eutardigrada; Ramazzottiidae) and their evolutionary relationships. Syst Biodivers 17:573–593. https://doi.org/10.1080/14772000.2019.1649737
Guil N, Giribet G (2012) A comprehensive molecular phylogeny of tardigrades—adding genes and taxa to a poorly resolved phylum-level phylogeny. Cladistics 28:21–49. https://doi.org/10.1111/j.1096-0031.2011.00364.x
Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 52:696–704. https://doi.org/10.1080/10635150390235520
Gutzmann E, Martínez Arbizu P, Rose A, Veit-Köhler G (2004) Meiofauna communities along an abyssal depth gradient in the Drake Passage. Deep Sea Res II 51:1617–1628. https://doi.org/10.1016/j.dsr2.2004.06.026
Herman RL, Dahms HU (1992) Meiofauna communities along a depth transect off Halley Bay (Weddell Sea-Antarctica). Polar Biol 12:313–320. https://doi.org/10.1007/BF00238274
Jørgensen A, Faurby S, Hansen JG, Møbjerg N, Kristensen RM (2010) Molecular phylogeny of Arthrotardigrada (Tardigrada). Mol Phylogenet Evol 54:1006–1015. https://doi.org/10.1016/j.ympev.2009.10.006
Kaczmarek Ł, Janko K, Smykla J, Michalczyk Ł (2014) Soil tardigrades from the Antarctic Peninsula with a description of a new species and some remarks on the genus Ramajendas (Eutardigrada, Isohypsibiidae). Polar Rec 50:176–182. https://doi.org/10.1017/S0032247413000168
Kaczmarek Ł, Bartels PJ, Roszkowska M, Nelson DR (2015) The zoogeography of marine Tardigrada. Zootaxa 4037:1–189. https://doi.org/10.11646/zootaxa.4037.1.1
Kaczmarek Ł, Parnikoza I, Gawlak M, Esefeld J, Peter H-U, Kozeretska I, Roszkowska M (2018) Tardigrades from Larus dominicanus Lichtenstein, 1823 nests on the Argentine Islands (maritime Antarctic). Polar Biol 41:283–301. https://doi.org/10.1007/s00300-017-2190-4
Kaczmarek Ł, Mioduchowska M, Kačarević U, Kubska K, Parnikoza I, Gołdyn B, Roszkowska M (2020) New records of Antarctic Tardigrada with comments on interpopulation variability of the Paramacrobiotus fairbanksi Schill, Förster, Dandekar and Wolf, 2010. Diversity 12:108. https://doi.org/10.3390/d12030108
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on faster Fourier transform. Nucleic Acids Res 30:3059–3066. https://doi.org/10.1093/nar/gkf436
Kristensen RM, Higgins RP (1984) Revision of Styraconyx (Tardigrada: Halechiniscidae) with description of two new species from Disko Bay, West Greenland. Smithson Contrib Zool 391:1–40. https://doi.org/10.5479/si.00810282.391
Kristensen RM, Renaud-Mornant J (1983) Existence d’arthrotardigrades semi-benthiques de genres nouveaux de la sousfamille des Styraconyxinae subfam. nov. Cah Biol Mar 24:337–353
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Markmann M, Tautz D (2005) Reverse taxonomy: an approach towards determining the diversity of meiobenthic organisms based on ribosomal RNA signature sequences. Philos Trans R Soc B 360:1917–1924. https://doi.org/10.1098/rstb.2005.1723
Miller R, Kristensen RM (1999) Tardigrades of the Australian Antarctic: a new species of the marine genus Echiniscoides from Macquarie Island, Subantarctica. Zool Anz 238:289–294
Noda H (1994) Tardigrades from sand beaches in Okinawa. Proc Jpn Soc Syst Zool 51:79 conference abstract in Japanese
O’Leary MA, Kaufman SG (2012) MorphoBank 3.0: web application for morphological phylogenetics and taxonomy. https://www.morphobank.org. Accessed 4 July 2019
Ramazzotti G (1972) Tardigradi delle isole Kerguelen e discrizione della nuova specie Hypsibius (I.) renaudi. Mem Ist Ital Idrobiol 29:141–144
Riesgo A, Taboada S, Avila C (2015) Evolutionary patterns in Antarctic marine invertebrates: an update on molecular studies. Mar Genomics 23:1–13
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. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Sáiz-Salinas JI, Ramos A, García FJ, Troncoso JS, San Martin G, Sanz C, Palacin C (1997) Quantitative analysis of macrobenthic soft-bottom assemblages in South Shetland waters (Antarctica). Polar Biol 17:393–400. https://doi.org/10.1007/PL00013382
Stamatakis A (2014) RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Steiner G (1926) Bathyechiniscus tetronyx n.g. n.sp. Ein neuer mariner tardigrade. Deutsche Südpolar-Expedition 18. Zoology 10:477–481
Tang CQ, Leasi F, Obertegger U, Kieneke A, Barraclough TG, Fontaneto D (2012) The widely used small subunit 18S rDNA molecule greatly underestimates true diversity in biodiversity surveys of the meiofauna. Proc Natl Acad Sci USA 109(40):16208–16212. https://doi.org/10.1073/pnas.1209160109
Vanhove S, Wittoeck J, Desmet G, Van den Berghe B, Herman RL, Bak RPM, Nieuwland G, Vosjan JH, Boldrin A, Rabitti S, Vincx M (1995) Deep-sea meiofauna communities in Antarctica: structural analysis and relation with the environment. Mar Ecol Prog Ser 127:65–76
Vanhove S, Lee HJ, Beghyn M, Van Gansbeke D, Brockington S, Vincx M (1998) The metazoan meiofauna in its biochemical environment: the case of an Antarctic coastal sediment. J Mar Biol Assoc UK 78:411–434
Vecchi M, Cesari M, Bertolani R, Jönsson KI, Rebecchi L, Guidetti R (2016) Integrative systematic studies on tardigrades from Antarctica identify new genera and new species within Macrobiotoidea and Echiniscoidea. Invertebr Syst 30:303–322. https://doi.org/10.1071/IS15033
Veit-Köhler G, Durst S, Schuckenbrock J, Hauquier F, Durán Suja L, Dorschel B, Vanreusel A, Martínez Arbizu P (2018) Oceanographic and topographic conditions structure benthic meiofauna communities in the Weddell Sea, Bransfield Strait and Drake Passage (Antarctic). Prog Oceanogr 162:240–256. https://doi.org/10.1016/j.pocean.2018.03.005
Velasco-Castrillón A, Gibson JAE, Stevens MI (2014) A review of current Antarctic limno-terrestrial microfauna. Polar Biol 37:1517–1531. https://doi.org/10.1007/s00300-014-1544-4
Villora-Moreno S (1998) Deep-sea Tardigrada from South Shetland Islands (Antarctica) with description of Angursa antarctica sp. nov. (Arthrotardigrada, Halechiniscidae). Polar Biol 19:336–341. https://doi.org/10.1007/s003000050255
Wessel P, Smith WHF, Scharroo R, Luis J, Wobbe F (2013) Generic mapping tools: improved version released. Eos Trans AGU 94:409–410. https://doi.org/10.1002/2013EO450001
Acknowledgements
We sincerely acknowledge the master and crew of the icebreaker Shirase and the observation members and supporting members of JARE59 for their great contribution to the field operation. We would also like to thank Paul Bartels, Sandra McInnes, and one anonymous reviewer for their helpful comments to improve the manuscript. This study is a part of JARE 59 supported by NIPR and the result of the research meeting held there in December 2018. This study was also supported by the Research Project Fund of the Research and Education Center for Natural Science, Keio University, NIPR through General Collaboration Project No. 28-43, JSPS Grant-in-Aid for Scientific Research (JP25241001, JP17H01615), and MEXT Grant-in-Aid for Scientific Research (JP17H06322).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Fujimoto, S., Suzuki, A.C., Ito, M. et al. Marine tardigrades from Lützow-Holm Bay, East Antarctica with the description of a new species. Polar Biol 43, 679–693 (2020). https://doi.org/10.1007/s00300-020-02671-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-020-02671-w