An integrative redescription of Echiniscus quadrispinosus quadrispinosus Richters, 1902 (Heterotardigrada, Echiniscidae) from the terra typica in Taunus Mountain Range (Europe; Germany)

  • Łukasz Kaczmarek Department of Animal Taxonomy and Ecology, Faculty of Biology, Adam Mickiewicz University in Poznań, Uniwersytetu Poznańskiego 6, 61-614 Poznań, Poland
  • Pushpalata Kayastha Department of Animal Taxonomy and Ecology, Faculty of Biology, Adam Mickiewicz University in Poznań, Uniwersytetu Poznańskiego 6, 61-614 Poznań, Poland
  • Magdalena Gawlak The Institute of Plant Protection-National Research Institute, Węgorka 20, 60-318 Poznań, Poland
  • Monika Mioduchowska Department of Evolutionary Genetics and Biosystematics, Faculty of Biology, University of Gdansk, Wita Stwosza 59, 80-308 Gdansk, Poland
  • Milena Roszkowska Department of Animal Taxonomy and Ecology, Faculty of Biology, Adam Mickiewicz University in Poznań, Uniwersytetu Poznańskiego 6, 61-614 Poznań, Poland
Keywords: E. lichenorum Maucci, 1983, E. q. brachyspinosus Bartoš, 1934, E. q. cribrosus Murray, 1907, E. q. fissispinosus Murray, 1907, Tardigrada

Abstract

In the present study, we used an integrative taxonomy approach to redescribe a population of Echiniscus quadrispinosus quadrispinosus Richters, 1902 from the neotype locality in the Taunus Mountain Range (Germany). We found clear differences in the chaetotaxy formula between the life stages of E. q. quadrispinosus. The body appendages B are, in general, absent in juveniles. Moreover, in larvae all body lateral appendages, except for E, are absent. We also obtained DNA sequences of 18S rRNA, 28S rRNA, ITS-2, and COI of E. q. quadrispinosus from the neotype locality and three Norwegian populations. Comparison with the sequences available in GenBank showed low genetic differences between the neotypic population and specimens from other localities. Therefore, we decided to establish our specimens from Taunus Mountain Range as neotype and paraneotypes of E. q. quadrispinosus. We also discussed and amended the taxonomic status of three subspecies E. q. brachyspinosus Bartoš, 1934, E. q. cribrosus Murray, 1907 and E. q. fissispinosus Murray, 1907 and established them as junior synonyms of E. q. quadrispinosus. Finally, we also confirmed E. lichenorum Maucci, 1983 as a valid species, clearly different from E. q. quadrispinosus.

References

Altschul S.F., Gish W., Miller W., Myers E.W. & Lipman D.J. 1990. Basic local alignment search tool. Journal of Molecular Biology 215 (3): 403–410. https://doi.org/10.1016/S0022-2836(05)80360-2

Bartoš E. 1934. Prispevek k Poznani Tardigrad ČSR. Časopis Československé Společnosti Entomologické 31: 99–107.

Bartylak T., Kulpa A., Grobys D., Kepel M., Kepel A., Kmita H., Gawlak M., Grabiński W., Roszkowska M. & Kaczmarek Ł. 2019. Variability of Echiniscus tristis Gąsiorek & Kristensen, 2018—is morphology sufficient for taxonomic differentiation of Echiniscidae? Zootaxa 4701 (1): 1–24. https://doi.org/10.11646/zootaxa.4701.1.1

Bochnak M., Vončina K., Kristensen R.M. & Gasiorek P. 2020. Continued exploration of Tanzanian rainforests reveals a new echiniscid species (Heterotardigrada). Zoological Studies 59: 18. https://doi.org/10.6620/ZS.2020.59-18

Casquet J., Thebaud C. & Gillespie R.G. 2012. Chelex without boiling, a rapid and easy technique to obtain stable amplifiable DNA from small amounts of ethanol-stored spiders. Molecular Ecology Resources 12 (1): 136–141. https://doi.org/10.1111/j.1755-0998.2011.03073.x

Claxton S.K. 1996. Sexual dimorphism in Australian Echiniscus (Tardigrada, Echiniscidae) with description of three new species. Zoological Journal of the Linnean Society 116 (1–2): 13–33. https://doi.org/10.1111/j.1096-3642.1996.tb02330.x

Claxton S.K. & Dastych H. 2017. A new bisexual species of Echiniscus C.A.S. Schultze, 1840 (Heterotardigrada: Echiniscidae) from Tasmania, Australia. Entomologie heute 29: 105–119.

Cuénot L. 1932. Tardigrades. In: Lechevalier P. (ed.) Faune de France 24: 1–96.

Dastych H. 1980. Niesporczaki (Tardigrada) Tatrzańskiego Parku Narodowego. Monografie Fauny Polski 9: 1–232.

Dastych H. 1999. A new species of the genus Mopsechiniscus Du Bois-Reymond Marcus, 1944 (Tardigrada) from the Venezuelan Andes. Acta Biologica Benrodis 10: 91–101.

Degma P. & Guidetti R. 2007. Notes to the current checklist of Tardigrada. Zootaxa 1579 (1): 41–53. https://doi.org/10.11646/zootaxa.1579.1.2

Degma P., Bertolani R. & Guidetti R. 2009–2021. Actual checklist of Tardigrada species. (2009–2021, 40th Edition: 19–07–2021). Available from https://iris.unimore.it/retrieve/358743/Actual%20checklist%20of%20Tardigrada%2040th%20Edition%2019-07-21.pdf [accessed 4 May 2022].

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 (5): 294–299.

Fontoura P. & Morais P. 2011. Assessment of traditional and geometric morphometrics for discriminating cryptic species of the Pseudechiniscus suillus complex (Tardigrada, Echiniscidae). Journal of Zoological Systematics and Evolutionary Research 49 (s1): 26–33. https://doi.org/10.1111/j.1439-0469.2010.00594.x

Gąsiorek P. & Kristensen R.M. 2018. Echiniscidae (Heterotardigrada) of Tanzania and Uganda. Tropical Zoology 31 (3): 131–160. https://doi.org/10.1080/03946975.2018.1477350

Gąsiorek P. & Michalczyk Ł. 2020a. Revised Cornechiniscus (Heterotardigrada) and new phylogenetic analyses negate echiniscid subfamilies and tribes. Royal Society Open Science 7 (6): 200581. https://doi.org/10.1098/rsos.200581

Gąsiorek P. & Michalczyk Ł. 2020b. Echiniscus siticulosus (Echiniscidae: spinulosus group), a new tardigrade from Western Australian scrub. New Zealand Journal of Zoology 47 (2): 87–105. https://doi.org/10.1080/03014223.2019.1603166

Gąsiorek P. & Vončina K. 2019. New Echiniscidae (Heterotardigrada) from Amber Mountain (Northern Madagascar). Evolutionary Systematics 3 (1): 29–39. https://doi.org/10.3897/evolsyst.3.33580

Gąsiorek P., Stec D., Morek W. & Michalczyk Ł. 2017. An integrative redescription of Echiniscus testudo (Doyère, 1840), the nominal taxon for the class Heterotardigrada (Ecdysozoa: Panarthropoda: Tardigrada). Zoologischer Anzeiger 270: 107–122. https://doi.org/10.1016/j.jcz.2017.09.006

Gąsiorek P., Morek W., Stec D. & Michalczyk Ł. 2019a. Untangling the Echiniscus Gordian knot: paraphyly of the “arctomys group” (Heterotardigrada: Echiniscidae). Cladistics 35 (6): 633–653. https://doi.org/10.1111/cla.12377

Gąsiorek P., Jackson K.J., Meyer H.A., Zając K., Nelson D.R., Kristensen R.M. & Michalczyk Ł. 2019b. Echiniscus virginicus complex: the first case of pseudocryptic allopatry and pantropical distribution in tardigrades. Biological Journal of the Linnean Society 128 (4): 789–805. https://doi.org/10.1093/biolinnean/blz147

Gąsiorek P., Vončina K. & Michalczyk Ł. 2019c. Echiniscus testudo (Doyère, 1840) in New Zealand: anthropogenic dispersal or evidence for the ‘Everything is Everywhere’ hypothesis? New Zealand Journal of Zoology 46 (2): 174–181. https://doi.org/10.1080/03014223.2018.1503607

Gąsiorek P., Vončina K. & Michalczyk Ł. 2020. An overview of the sexual dimorphism in Echiniscus (Heterotardigrada, Echiniscoidea), with the description of Echiniscus masculinus sp. nov. (the virginicus complex) from Borneo. Zoosystematics and Evolution 96 (1): 103–113. https://doi.org/10.3897/zse.96.49989

Goujon M., Mcwilliam H., Li W., Valentin F., Squizzato S., Paern J. & Lopez R. 2010. A new bioinformatics analysis tools framework at EMBL–EBI. Nucleic Acids Research 38 (Suppl. 2): 695–699. https://doi.org/10.1093/nar/gkq313

Guidetti R. & Bertolani R. 2005. Tardigrade taxonomy: an updated check list of the taxa and a list of characters for their identification. Zootaxa 845 (1): 1–46. https://doi.org/10.11646/zootaxa.845.1.1

Guidetti R., Schill R.O., Bertolani R., Dandekar T. & Wolf M. 2009. New molecular data for tardigrade phylogeny, with the erection of Paramacrobiotus gen. nov. Journal of Zoological Systematics and Evolutionary Research 47 (4): 315–321. https://doi.org/10.1111/j.1439-0469.2009.00526.x

Guil N. 2008. New records and within-species variability of Iberian tardigrades (Tardigrada), with comments on the species from the Echiniscus blumi-canadensis series. Zootaxa 1757 (1): 1–30. https://doi.org/10.11646/zootaxa.1757.1.1

Guil N. & Giribet G. 2012. A comprehensive molecular phylogeny of tardigrades — adding genes and taxa to a poorly resolved phylum-level phylogeny. Cladistics 28 (1): 21–49. https://doi.org/10.1111/j.1096-0031.2011.00364.x

Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium 41: 95–98. Available from http://brownlab.mbio.ncsu.edu/JWB/papers/1999Hall1.pdf [accessed 4 May 2022].

Jørgensen A., Møbjerg N. & Kristensen R.M. 2007. A molecular study of the tardigrade Echiniscus testudo (Echiniscidae) reveals low DNA sequence diversity over a large geographical area. Journal of Limnology 66 (1s): 77–83. https://doi.org/10.4081/jlimnol.2007.s1.77

Jørgensen A., Faurby S., Hansen J.G., Møbjerg N., Mobjerg N. & Kristensen R.M. 2010. Molecular phylogeny of Arthrotardigrada (Tardigrada). Molecular Phylogenetics and Evolution 54 (3): 1006–1015. https://doi.org/10.1016/j.ympev.2009.10.006

Jørgensen A., Møbjerg N. & Kristensen R.M. 2011. Phylogeny and evolution of the Echiniscidae (Echiniscoidea, Tardigrada) – an investigation of the congruence between molecules and morphology. Journal of Zoological Systematics and Evolutionary Research 49 (1): 6–16. https://doi.org/10.1111/j.1439-0469.2010.00592.x

Kaczmarek Ł. & Michalczyk Ł. 2010. The genus Echiniscus Schultze 1840 (Tardigrada) in Costa Rican (Central America) rain forests with descriptions of two new species. Tropical Zoology 23 (1): 91–106.

Kaczmarek Ł., Michalczyk Ł. & McInnes S.J. 2016. Annotated zoogeography of non-marine Tardigrada. Part III: North America and Greenland. Zootaxa 4203 (1): 1–249. https://doi.org/10.11646/zootaxa.4203.1.1

Kaczmarek Ł., Grobys D., Kulpa A., Bartylak T., Kmita H., Kepel M., Kepel A. & Roszkowska M. 2019. Two new species of the genus Milnesium Doyère, 1840 (Tardigrada, Apochela, Milnesiidae) from Madagascar. ZooKeys 884: 1–22. https://doi.org/10.3897/zookeys.884.29469

Kayastha P., Berdi D., Mioduchowska M., Gawlak M., Łukasiewicz A., Gołdyn B., Jędrzejewski S. & Kaczmarek Ł. 2020. Description and molecular characterization of Richtersius ziemowiti sp. nov. (Richtersiidae) from Nepal (Asia) with evidence of heterozygous point mutation events in the 28S rRNA. Annales Zoologici 70 (3): 381–396. https://doi.org/10.3161/00034541ANZ2020.70.3.010

Kiosya Y., Vončina K. & Gąsiorek P. 2021. Echiniscidae in the Mascarenes: the wonders of Mauritius. Evolutionary Systematics 5 (1): 93–120. https://doi.org/10.3897/evolsyst.5.59997

Kristensen R.M. 1987. Generic revision of the Echiniscidae (Heterotardigrada), with a discussion of the origin of the family. In: Bertolani, R. (ed.) Biology of Tardigrada. Selected Symposia and Monographs: 261–335. U.Z.I. Mucci, Modena.

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

Librado P. & Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25 (11): 1451–1452. https://doi.org/10.1093/bioinformatics/btp187

McInnes S.J. 1994. Zoogeographic distribution of terrestrial/freshwater tardigrades from current literature. Journal of Natural History 28 (2): 257–352. https://doi.org/10.1080/00222939400770131

McInnes S.J., Michalczyk Ł. & Kaczmarek Ł. 2017. Annotated zoogeography of non-marine Tardigrada. Part IV: Africa. Zootaxa 4284 (1): 1–74. https://doi.org/10.11646/zootaxa.4284.1.1

Meyer H.A. 2013. Terrestrial and freshwater Tardigrada of the Americas. Zootaxa 3747 (1): 1–71. https://doi.org/10.11646/zootaxa.3747.1.1

Michalczyk Ł. & Kaczmarek Ł. 2013. The Tardigrada Register: a comprehensive online data repository for tardigrade taxonomy. Journal of Limnology 72 (S1): 175–181. https://doi.org/10.4081/jlimnol.2013.s1.e22

Mironov S.V., Dabert J. & Dabert M. 2012. A new feather mite species of the genus Proctophyllodes Robin, 1877 (Astigmata: Proctophyllodidae) from the Long-tailed Tit Aegithalos caudatus (Passeriformes: Aegithalidae) — morphological description with DNA barcode data. Zootaxa 3253 (1): 54–61. https://doi.org/10.11646/zootaxa.3253.1.2

Murray J. 1907. Scottish Tardigrada collected by the Lake Survey. Transactions of the Royal Society of Edinburgh 45 (3): 641–668. https://doi.org/10.1017/S0080456800011777

Nelson D.R., Guidetti R., Rebecchi L., Kaczmarek Ł. & McInnes S.J. 2020. Phylum Tardigrada. In: Damborenea C., Rogers D.C. & Thorp T. (eds) Thorp and Covich’s Freshwater Invertebrates 4th Ed., Vol. 5. Keys to Neotropical and Antarctic Fauna 5: 505–522. https://doi.org/10.1016/B978-0-12-804225-0.00015-0

Ramazzotti G. & Maucci W. 1983. Il Phylum Tardigrada. III edizione riveduta e aggiornata. Memorie dell′Istituto Italiano di Idrobiologia, Pallanza 41: 1–1012.

Rice P., Longden I. & Bleasby A. 2000. EMBOSS: the European Molecular Biology Open Software Suite. Trends in Genetics 16: 276–277. https://doi.org/10.1016/S0168-9525(00)02024-2

Richters F. 1902. Neue Moosbewohner. Bericht der Senckenbergischen Naturforschenden Gesellschaft in Frankfurt am Main 1902: 23–26. Available from https://www.biodiversitylibrary.org/page/8478822 [accessed 4 May 2022].

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

Sands C.J., McInnes S.J., Marley N.J., Goodall-Copestake W.P., Convey P. & Linse K. 2008. Phylum Tardigrada: an “individual” approach. Cladistics 24 (6): 861–871. https://doi.org/10.1111/j.1096-0031.2008.00219.x

Schill R.O. & Steinbrück G. 2007. Identification and differentiation of Heterotardigrada and Eutardigrada species by riboprinting. Journal of Zoological Systematics and Evolutionary Research 45 (3): 184–190. https://doi.org/10.1111/j.1439-0469.2007.00409.x

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 Research 22 (22): 4673–4680. https://doi.org/10.1093/nar/22.22.4673

Vecchi M., Newton I.L., Cesari M., Rebecchi L. & Guidetti R. 2018. The microbial community of tardigrades: environmental influence and species specificity of microbiome structure and composition. Microbial Ecology 76 (2): 467–481. https://doi.org/10.1007/s00248-017-1134-4

Vicente F. & Bertolani R. 2013. Considerations on the taxonomy of the Phylum Tardigrada. Zootaxa 3626 (2): 245–248. https://doi.org/10.11646/zootaxa.3626.2.2

Vicente F., Cesari M., Serrano A. & Bertolani R. 2013. The impact of fire on terrestrial tardigrade biodiversity: a first case-study from Portugal. Journal of Limnology 72 (S1): 152–159. https://doi.org/10.4081/jlimnol.2013.s1.e19

White T.J., Bruns T., Lee S. & Taylor J. 1990. 38 – Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M.A., Gelfand D.H., Sninsky J.J. & White T.J. (eds) PCR Protocols: A Guide to Methods and Applications: 315–322. Academic Press, San Diego, CA. https://doi.org/10.1016/B978-0-12-372180-8.50042-1

Published
2022-06-14
How to Cite
Kaczmarek, Łukasz, Kayastha, P., Gawlak, M., Mioduchowska, M., & Roszkowska, M. (2022). An integrative redescription of Echiniscus quadrispinosus quadrispinosus Richters, 1902 (Heterotardigrada, Echiniscidae) from the terra typica in Taunus Mountain Range (Europe; Germany) . European Journal of Taxonomy, 823(1), 102–124. https://doi.org/10.5852/ejt.2022.823.1819
Section
Research article