Untangling the Echiniscus Gordian knot: Stellariscus gen. nov. (Heterotardigrada : Echiniscidae) from Far East Asia
Piotr Gąsiorek A D , Atsushi C. Suzuki B , Reinhardt M. Kristensen C , Dorota Lachowska-Cierlik A and Łukasz Michalczyk AA Department of Entomology, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387 Kraków, Poland.
B Department of Biology, Keio University, Yokohama 223-8521, Japan.
C Section of Biosystematics, Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark.
D Corresponding author. Email: piotr.lukas.gasiorek@gmail.com
Invertebrate Systematics 32(5) 1234-1247 https://doi.org/10.1071/IS18023
Submitted: 10 March 2018 Accepted: 22 May 2018 Published: 17 October 2018
Abstract
Species constituting the family Echiniscidae are highly derived, armoured and inhabit terrestrial habitats, in contrast to other heterotardigrades that are predominantly marine. The genus Echiniscus C.A.S. Schultze, 1840, nominal for the family Echiniscidae, is currently the most speciose tardigrade genus. However, the great morphological variability, in comparison with other heterotardigrade genera, suggests the polyphyletic character of the genus. Here, we analyse new specimens of Echiniscus pseudelegans Séméria, 1994 collected in Japan and conclude that the species as well as two other related taxa, E. elegans Richters, 1907 and E. latifasciatus Dudichev and Biserov, 2000, represent a new genus, Stellariscus, gen. nov. The new genus is characterised by a mixture of peculiar morphological apomorphies: black eyes, star-like dorsal plate sculpturing, no trunk appendages (only cephalic cirri present), two types of ventral plates, and striking sexual dimorphism in both qualitative and quantitative traits. Morphological phylogeny of the family Echiniscidae suggests a close affinity between Stellariscus, Hypechiniscus Thulin, 1928 and Pseudechiniscus Thulin, 1911. The polyphyletic status of both Echiniscus and Testechiniscus Kristensen, 1987 is also inferred. The taxonomic significance of ventral armature in echiniscid phylogeny and taxonomy is discussed.
Additional keywords: cuticle, Echiniscoidea, morphology, phylogeny, polyphyly, sexual dimorphism, ventral plates.
References
Bremer, K. (1994). Branch support and tree stability. Cladistics 10, 295–304.| Branch support and tree stability.Crossref | GoogleScholarGoogle Scholar |
Claxton, S. K. (1996). Sexual dimorphism in Australian Echiniscus (Tardigrada, Echiniscidae) with descriptions of three new species. Zoological Journal of the Linnean Society 116, 13–33.
| Sexual dimorphism in Australian Echiniscus (Tardigrada, Echiniscidae) with descriptions of three new species.Crossref | GoogleScholarGoogle Scholar |
Claxton, S. K. (2001). Antechiniscus in Australia: description of Antechiniscus moscali sp. n. and redescription of Antechiniscus parvisentus (Horning & Schuster, 1983) (Heterotardigrada: Echiniscidae). Zoologischer Anzeiger 240, 281–289.
| Antechiniscus in Australia: description of Antechiniscus moscali sp. n. and redescription of Antechiniscus parvisentus (Horning & Schuster, 1983) (Heterotardigrada: Echiniscidae).Crossref | GoogleScholarGoogle Scholar |
Dastych, H. (1986). Echiniscus rackae sp. n., a new species of Tardigrada from the Himalayas. Entomologische Mitteilungen aus dem Zoologischen Museum Hamburg 8, 246–250.
Dastych, H., McInnes, S. J., and Claxton, S. K. (1998). Oreella mollis Murray, 1910 (Tardigrada): a redescription and revision of Oreella. Mitteilungen aus den Hamburgischen Zoologischen Museum und Institut, Hamburg 95, 89–113.
Degma, P., and Guidetti, R. (2007). Notes to the current checklist of Tardigrada. Zootaxa 1579, 41–53.
Degma, P., Bertolani, R., and Guidetti, R. (2009–2018). Actual checklist of Tardigrada species. 34th edition. www.tardigrada.modena.unimo.it/miscellanea/Actual%20checklist%20of%20Tardigrada.pdf [Accessed 2 July 2018].
Doyère, M. L. (1840). Mémorie sur les tardigrades. Annales des Sciences Naturelles, Paris, Series 2 14, 269–362.
du Bois-Reymond Marcus, E. (1944). Sobre tardígrados Brasileiros. Comunicaciones Zoologicas del Museo de Historia Natural de Montevideo 1, 1–19.
Dudichev, A. L., and Biserov, V. I. (2000). Tardigrades (Tardigrada) from Iturup and Paramushir, the Kuril Islands. Зоологический журнал 79, 771–778.
Fontoura, P., and 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, 26–33.
| Assessment of traditional and geometric morphometrics for discriminating cryptic species of the Pseudechiniscus suillus complex (Tardigrada, Echiniscidae).Crossref | GoogleScholarGoogle Scholar |
Fontoura, P., Bartels, P. J., Jørgensen, A., Kristensen, R. M., and Hansen, J. G. (2017). A dichotomous key to the genera of the marine heterotardigrades (Tardigrada). Zootaxa 4294, 1–45.
| A dichotomous key to the genera of the marine heterotardigrades (Tardigrada).Crossref | GoogleScholarGoogle Scholar |
Gąsiorek, P. (2018). New Bryodelphax species (Heterotardigrada: Echiniscidae) from Western Borneo (Sarawak), with new molecular data for the genus. Raffles Bulletin of Zoology 66, 371–381.
Gąsiorek, P., and Degma, P. (2018). Three Echiniscidae species (Tardigrada: Heterotardigrada) new to the Polish fauna, with the description of a new gonochoristic Bryodelphax Thulin, 1928. Zootaxa 4410, 77–96.
| Three Echiniscidae species (Tardigrada: Heterotardigrada) new to the Polish fauna, with the description of a new gonochoristic Bryodelphax Thulin, 1928.Crossref | GoogleScholarGoogle Scholar |
Gąsiorek, P., Stec, D., Morek, W., Marnissi, J., and Michalczyk, Ł. (2017a). The tardigrade fauna of Tunisia, with an integrative description of Bryodelphax maculatus sp. nov. (Heterotardigrada: Echiniscidae). African Zoology 52, 77–89.
| The tardigrade fauna of Tunisia, with an integrative description of Bryodelphax maculatus sp. nov. (Heterotardigrada: Echiniscidae).Crossref | GoogleScholarGoogle Scholar |
Gąsiorek, P., Stec, D., Morek, W., and Michalczyk, Ł. (2017b). An integrative redescription of Echiniscus testudo (Doyère, 1840), the nominal taxon for the class Heterotardigrada (Ecdysozoa: Panarthropoda: Tardigrada). Zoologischer Anzeiger 270, 107–122.
| An integrative redescription of Echiniscus testudo (Doyère, 1840), the nominal taxon for the class Heterotardigrada (Ecdysozoa: Panarthropoda: Tardigrada).Crossref | GoogleScholarGoogle Scholar |
Goloboff, P. A., Farris, J. S., and Nixon, K. C. (2008). TNT, a free program for phylogenetic analysis. Cladistics 24, 774–786.
| TNT, a free program for phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar |
Guidetti, R., Rebecchi, L., and Bertolani, R. (2000). Cuticle structure and systematics of the Macrobiotidae (Tardigrada, Eutardigrada). Acta Zoologica (Stockholm) 81, 27–36.
| Cuticle structure and systematics of the Macrobiotidae (Tardigrada, Eutardigrada).Crossref | GoogleScholarGoogle Scholar |
Guil, N., Jørgensen, A., Giribet, G., and Kristensen, R. M. (2013). Congruence between molecular phylogeny and cuticular design in Echiniscoidea (Tardigrada, Heterotardigrada). Zoological Journal of the Linnean Society 169, 713–736.
| Congruence between molecular phylogeny and cuticular design in Echiniscoidea (Tardigrada, Heterotardigrada).Crossref | GoogleScholarGoogle Scholar |
Hansen, J. G., Kristensen, R. M., and Jørgensen, A. (2012). The armoured marine tardigrades (Arthrotardigrada, Tardigrada). Scientia Danica, Series B. Biologica 2, 1–92.
Hansen, J. G., Kristensen, R. M., Jørgensen, A., Accogli, G., D’Addabbo, R., and Gallo, M. (2016). Postembryonic development, paedomorphosis, secondary sexual dimorphism and population structure of a new Florarctus species (Tardigrada, Heterotardigrada). Zoological Journal of the Linnean Society 178, 871–877.
| Postembryonic development, paedomorphosis, secondary sexual dimorphism and population structure of a new Florarctus species (Tardigrada, Heterotardigrada).Crossref | GoogleScholarGoogle Scholar |
Jørgensen, A. (2000). Cladistic analysis of Echiniscidae Thulin, 1928 (Tardigrada: Heterotardigrada: Echiniscoidea). Steenstrupia (Copenhagen) 25, 11–23.
Jørgensen, A., Møbjerg, N., and 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, 6–16.
| Phylogeny and evolution of the Echiniscidae (Echiniscoidea, Tardigrada) – an investigation of the congruence between molecules and morphology.Crossref | GoogleScholarGoogle Scholar |
Kaczmarek, Ł., Zawierucha, K., Smykla, J., and Michalczyk, Ł. (2012). Tardigrada of the Revdalen (Spitsbergen) with the descriptions of two new species: Bryodelphax parvuspolaris (Heterotardigrada) and Isohypsibius coulsoni (Eutardigrada). Polar Biology 35, 1013–1026.
| Tardigrada of the Revdalen (Spitsbergen) with the descriptions of two new species: Bryodelphax parvuspolaris (Heterotardigrada) and Isohypsibius coulsoni (Eutardigrada).Crossref | GoogleScholarGoogle Scholar |
Kim, H. S., and Moon, S. N. (1988). Terrestrial Heterotardigrada (Tardigrada) from Korea. Korean Journal of Systematic Zoology 4, 47–56.
Kristensen, R. M. (1987). Generic revision of the Echiniscidae (Heterotardigrada), with a discussion of the origin of the family. Biology of Tardigrades. Selected Symposia and Monographs U.Z.I. 1, 261–335.
Maucci, W., and Ramazzotti, G. (1981). Cornechiniscus gen. nov.: nuova posizione sistematica per i cosiddetti Pseudechiniscus gruppo cornutus, con descrizione di una nuova specie (Tardigrada, Echiniscidae). Memorie dell’Istituto Italiano di Idrobiologia, Pallanza 39, 147–151.
Michalczyk, Ł., and Kaczmarek, Ł. (2013). The Tardigrada Register: a comprehensive online data repository for tardigrade taxonomy. Journal of Limnology 72, 175–181.
| The Tardigrada Register: a comprehensive online data repository for tardigrade taxonomy.Crossref | GoogleScholarGoogle Scholar |
Morek, W., Stec, D., Gąsiorek, P., Schill, R. O., Kaczmarek, Ł., and Michalczyk, Ł. (2016). An experimental test of tardigrade preparation methods for light microscopy. Zoological Journal of the Linnean Society 178, 785–793.
| An experimental test of tardigrade preparation methods for light microscopy.Crossref | GoogleScholarGoogle Scholar |
Ramazzotti, G., and Maucci, W. (1983). Il Phylum Tardigrada. III Edizione riveduta e aggiornata. Memorie dell’Istituto Italiano di Idrobiologia 41, 1–1012.
Richters, F. (1903). Nordische tardigraden. Zoologischer Anzeiger 27, 168–172.
Richters, F. (1904). Arktische tardigraden. Fauna Arctica 3, 495–511.
Richters, F. (1907). Zwei neue Echiniscus-Arten. Zoologischer Anzeiger 31, 197–202.
Schulte, R., and Miller, W. R. (2011). Tardigrades of North America: the elevation of a new genus from California. Transactions of the Kansas Academy of Science 114, 177.
Séméria, Y. (1994). Une espèce nouvelle de tardigrade de Taiwan: Echiniscus pseudelegans, n. sp. (Heterotardigrada Echiniscidae). Bulletin Mensuel de la Societe Linneenne de Lyon 63, 28–30.
| Une espèce nouvelle de tardigrade de Taiwan: Echiniscus pseudelegans, n. sp. (Heterotardigrada Echiniscidae).Crossref | GoogleScholarGoogle Scholar |
Stec, D., Smolak, R., Kaczmarek, Ł., and Michalczyk, Ł. (2015). An integrative description of Macrobiotus paulinae sp. nov. (Tardigrada: Eutardigrada: Macrobiotidae: hufelandi group) from Kenya. Zootaxa 4052, 501–526.
| An integrative description of Macrobiotus paulinae sp. nov. (Tardigrada: Eutardigrada: Macrobiotidae: hufelandi group) from Kenya.Crossref | GoogleScholarGoogle Scholar |
Stec, D., Arakawa, K., and Michalczyk, Ł. (2018). An integrative description of Macrobiotus shonaicus sp. nov. (Tardigrada: Macrobiotidae) from Japan with notes on its phylogenetic position within the hufelandi group. PLoS One 13, .
| An integrative description of Macrobiotus shonaicus sp. nov. (Tardigrada: Macrobiotidae) from Japan with notes on its phylogenetic position within the hufelandi group.Crossref | GoogleScholarGoogle Scholar |
Suzuki, A. C. (2017). Tardigrade research in Japan. In ‘Species Diversity of Animals in Japan, Diversity and Commonality in Animals’. (Eds M. Motokawa and H. Kajihara.), pp. 267–284. (Springer: Tokyo, Japan.).
Vecchi, M., Cesari, M., Bertolani, R., Jönsson, K. I., Rebecchi, L., and Guidetti, R. (2016). Integrative systematic studies on tardigrades from Antarctica identify new genera and new species within Macrobiotoidea and Echiniscoidea. Invertebrate Systematics 30, 303–322.
| Integrative systematic studies on tardigrades from Antarctica identify new genera and new species within Macrobiotoidea and Echiniscoidea.Crossref | GoogleScholarGoogle Scholar |