Integrative description of Macrobiotus canaricus sp. nov. with notes on M. recens (Eutardigrada: Macrobiotidae)

  • Daniel Stec Department of Entomology, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387 Kraków
  • Łukasz Krzywański Department of Entomology, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387 Kraków
  • Łukasz Michalczyk Department of Entomology, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387 Kraków
Keywords: Canary Islands, COI, Macrobiotus hufelandi group, phylogeny, tardigrades

Abstract

In this paper we describe Macrobiotus canaricus sp. nov., a new tardigrade species of the Macrobiotus hufelandi group from the Canary Islands. Moreover, with the use of DNA sequencing, we confirm that Macrobiotus recens Cuénot, 1932 represents the hufelandi group, even though eggs laid by this species do not exhibit the typical hufelandi group morphology. Our study is based on both classical taxonomic methods that include morphological and morphometric analyses conducted with the use of light and scanning electron microscopy, and on the analysis of nucleotide sequences of four molecular markers (three nuclear: 18S rRNA, 28S rRNA, ITS-2, and one mitochondrial: COI). Our analyses revealed that M. canaricus sp. nov. is most similar to Macrobiotus almadai Fontoura et al., 2008 from the Archipelago of the Azores, from which it differs by the absence of granulation patches on the external and internal surfaces of legs I–III as well as by the absence of a cuticular pore in the centre of the external patch on legs I–III. Molecular sequences allowed us to pinpoint the phylogenetic positions of M. canaricus sp. nov. and M. recens within the M. hufelandi group.

References

Bartoš E. 1963. Die Tardigraden der chinesischen und javanischen Moosproben. Acta Societatis Zoologicae Bohemoslovenicae 27: 108–114.

Bertolani R. 1971. Rapporto-sessi e dimorfismo sessuale in Macrobiotus (Tardigrada). Rendiconti Accademia Nazionale Lincei 50 (8): 377–382.

Bertolani R. & Rebecchi L. 1993. A revision of the Macrobiotus hufelandi group (Tardigrada, Macrobiotidae), with some observations on the taxonomic characters of eutardigrades. Zoologica Scripta 22: 127–152. https://doi.org/10.1111/j.1463-6409.1993.tb00347.x

Bertolani R., Rebecchi L., Giovannini I. & Cesari M. 2011a. DNA barcoding and integrative taxonomy of Macrobiotus hufelandi C.A.S. Schultze 1834, the first tardigrade species to be described, and some related species. Zootaxa 2997: 19–36.

Bertolani R., Biserov V., Rebecchi L. & Cesari M. 2011b. Taxonomy and biogeography of tardigrades using an integrated approach: new results on species of the Macrobiotus hufelandi group. Invertebrate Zoology 8 (1): 23–36.

Bertolani R., Guidetti R., Marchioro T., Altiero T., Rebecchi L. & Cesari M. 2014. Phylogeny of Eutardigrada: New molecular data and their morphological support lead to the identification of new evolutionary lineages. Molecular Phylogenetics and Evolution 76: 110–126. https://doi.org/10.1016/j.ympev.2014.03.006

Binda M.G. & Pilato G. 1984. Macrobiotus sapiens, nuova specie di Eutardigrado di Sicilia. Animalia 11: 85–90.

Binda M.G. & Pilato G. 2001. Macrobiotus savai and Macrobiotus humilis, two new species of tardigrades from Sri Lanka. Bolletino delle Sedute dell’Accademia Gioenia di Scienze naturali in Catania 34: 101–111.

Biserov V.I. 1990a. On the revision of the genus Macrobiotus. The subgenus Macrobiotus sensu stricto: a new systematic status of the group hufelandi (Tardigrada, Macrobiotidae). Communication 1. Zoologicheskii Zhurnal 69 (12): 5–17.

Biserov V.I. 1990b. On the revision of the genus Macrobiotus. The subgenus Macrobiotus s. st. is a new systematic status of the hufelandi group (Tardigrada, Macrobiotidae). Communication 2. Zoologicheskii Zhurnal 69: 38–50.

Casquet J., Thebaud C. & Gillespie R. 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: 36–41. https://doi.org/10.1111/j.1755-0998.2011.03073.x

Cesari M., Bertolani R., Rebecchi L. & Guidetti R. 2009. DNA barcoding in Tardigrada: the first case study on Macrobiotus macrocalix Bertolani & Rebecchi 1993 (Eutardigrada, Macrobiotidae). Molecular Ecology Resources 9 (3): 699–706. https://doi.org/10.1111/j.1755-0998.2009.02538.x

Cesari M., Giovanni I., Bertolani R. & Rebecchi L. 2011. An example of problems associated with DNA barcoding in tardigrades: a novel method for obtaining voucher specimens. Zootaxa 3104: 42–51.

Dastych 1980. Niesporczaki (Tardigrada) Tatrzańskiego Parku Narodowego. Monografie Fauny Polski 9, Polskie Wydawnictwo Naukowe, Kraków.

Degma P. & Guidetti R. 2007. Notes to the current checklist of Tardigrada. Zootaxa 1579: 41–53.

Degma P., Bertolani R. & Guidetti R. 2009–2017. Actual checklist of Tardigrada species (2009–2017, 33rd Edition: 15-10-2017). Available from http://www.tardigrada.modena.unimo.it/miscellanea/Actual%20checklist%20of%20Tardigrada.pdf [accessed 23 Dec. 2017].

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.

Fontoura P., Pilato G. & Lisi O. 2008. New records of eutardigrades (Tardigrada) from Faial and Pico Islands, the Azores, with the description of two new species. Zootaxa 1778: 37–47.

Gąsiorek P., Stec D., Morek W. & Michalczyk Ł. 2018. An integrative redescription of Hypsibius dujardini (Doyère, 1840), the nominal taxon for Hypsibioidea (Tardigrada: Eutardigrada). Zootaxa 4415 (1): 45-75. https://doi.org/10.11646/zootaxa.4415.1.2

Giribet G., Carranza S., Baguña J., Riutort M. & Ribera C. 1996. First molecular evidence for the existence of a Tardigrada + Arthropoda clade. Molecular Biology and Evolution 13: 76–84. https://doi.org/10.1093/oxfordjournals.molbev.a025573

Grigarick A.A., Schuster R.O. & Torftner E.C. 1973. Descriptive morphology of eggs of some species in the Macrobiotus hufelandi group (Tardigrada: Macrobiotidae). Pan–Pacific Entomologist 49: 258–263.

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

Guidetti R., Gandolfi A., Rossi V. & Bertolani R. 2005. Phylogenetic analysis of Macrobiotidae (Eutardigrada, Parachela): a combined morphological and molecular approach. Zoologica Scripta 34: 235–244. https://doi.org/10.1111/j.1463-6409.2005.00193.x

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

Guidetti R., Peluffo J.R., Rocha A.M., Cesari M. & Moly de Peluffo M.C. 2013. The morphological and molecular analyses of a new South American urban tardigrade offer new insights on the biological meaning of the Macrobiotus hufelandi group of species (Tardigrada: Macrobiotidae). Journal of Natural History 47 (37–38): 2409–2426. https://doi.org/10.1080/00222933.2013.800610

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

Guil N. & Guidetti R. 2005. A new species of Tardigrada (Eutardigrada: Macrobiotidae) from Iberian Peninsula and Canary Islands (Spain). Zootaxa 889: 1–11. https://doi.org/10.11646/zootaxa.889.1.1

Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.

Heinis F. 1908. Beitrag zur Kenntnis der Moosfauna der Kanarischen Inseln. Zoologischer Anzeiger 33: 711–720.

Horning Jr. D.S., Schuster R.O. & Grigarick A.A. 1978. Tardigrada of New Zealand. New Zealand Journal of Zoology 5: 185–280. https://doi.org/10.1080/03014223.1978.10428316

Kaczmarek Ł. & Michalczyk Ł. 2017a. A description of Macrobiotus horningi sp. nov. and redescriptions of M. maculatus comb. nov. Iharos, 1973 and M. rawsoni Horning et al., 1978 (Tardigrada: Eutardigrada: Macrobiotidae: hufelandi group). Zootaxa 4363: 79–100. https://doi.org/10.11646/zootaxa.4363.1.3

Kaczmarek Ł. & Michalczyk Ł. 2017b. The Macrobiotus hufelandi group (Tardigrada) revisited. Zootaxa 4363: 101–123. https://doi.org/10.11646/zootaxa.4363.1.4

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

Katoh K. & Toh H. 2008. Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics 9: 286–298. https://doi.org/10.1093/bib/bbn013

Katoh K., Misawa K., Kuma K. & Mitaya T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30: 3059–66. https://doi.org/10.1093/nar/gkf436

Kumar S., Stecher G. & Taura 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

Lanfear R., Frandsen P.B., Wright A.M., Senfeld T. & Calcott B. 2016. PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34: 772–773. https://doi.org/10.1093/molbev/msw260

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.M. & 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.

Marcus E. 1936. Tardigrada. Das Tierreich 66: 1–340.

Marley N.J., McInnes S.J. & Sands C.J. 2011. Phylum Tardigrada: A re-evaluation of the Parachela. Zootaxa 2819: 51–64.

Maucci W. 1979. Osservazioni sul valore tassonomico di Macrobiotus recens Cuénot, 1932 (Tardigrada, Macrobiotidae). NATURA–Società italiana di Scienze naturale, Museo civico di Storia naturale e Acquatario civico, Milano 70: 258–264.

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.

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

Michalczyk Ł., Wełnicz W., Frohme M. & Kaczmarek Ł. 2012. Redescriptions of three Milnesium Doyère, 1840 taxa (Tardigrada: Eutardigrada: Milnesiidae), including the nominal species for the genus. Zootaxa 3154: 1–20.

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: 54–61.

Morek W., Gąsiorek P., Stec D., Bladgen B. & Michalczyk Ł. 2016a. Experimental taxonomy exposes ontogenetic variability and elucidates the taxonomic value of claw configuration in Milnesium Doyère, 1840 (Tardigrada: Eutardigrada: Apochela). Contributions to Zoology 85 (2): 173–200.

Morek W., Stec D., Gąsiorek P., Schill R.O., Kaczmarek Ł. & Michalczyk Ł. 2016b. 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., Guidetti R. & Rebecchi L. 2015. Phylum Tardigrada. In: Thorp J.H. & Rogers D.C. (eds) Ecology and General Biology. Vol. 1: Thorp and Covich’s Freshwater Invertebrates (4th edition): 347–380 (chapter 17). https://doi.org/10.1016/B978-0-12-385026-3.00017-6

Nowak B. & Stec D. 2018. An integrative description of Macrobiotus hannae sp. nov. (Tardigrada: Eutardigrada: Macrobiotidae: hufelandi group) from Poland. Turkish Journal of Zoology 42: 269–286. https://doi.org/10.3906/zoo-1712-31

Pilato G. 1981. Analisi di nuovi caratteri nello studio degli Eutardigradi. Animalia 8: 51–57.

Pilato G. & Bertolani R. 2004. Macrobiotus dariae sp. n., a new species of eutardigrade (Eutardigrada, Macrobiotidae) from Cyprus. Zootaxa 638: 1–7. https://doi.org/10.11646/zootaxa.638.1.1

Rahm G. 1937. Tardigraden vom Yan-Chia-Ping-Tal (Nordchina). Zoologischer Anzeiger 119: 105–111.

Ramazzotti G. 1945. I. Tardigradi d‘Italia. Memorie dell’Istituto italiano di Idrobiologia 2: 31–166.

Ramazzotti G. 1962. II. Phylum Tardigrada. Memorie dell’Istituto italiano di Idrobiologia 16: 1–595.

Ramazzotti G. 1972. Il Phylum Tardigrada (seconda edizione aggiornata). Memorie dell’Istituto italiano di Idrobiologia 28: 1–732.

Rambaut A., Drummond A.J., Xie D., Baele G. & Suchard M.A. 2018. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology syy032. https://doi.org/10.1093/sysbio/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., Ostrowska M., Stec D., Janko K. & Kaczmarek Ł. 2017. Macrobiotus polypiformis sp. nov., a new tardigrade (Macrobiotidae; hufelandi group) from the Ecuadorian Pacific coast, with remarks on the claw abnormalities in eutardigrades. European Journal of Taxonomy 327: 1–19. https://doi.org/10.5852/ejt.2017.327

Rudescu L. 1946. Tardigrada. Fauna Republicii Populare 4 (7), Academiei Republicii Populare Romini, Bucharest.

Sands C.J., McInnes S.J., Marley N.J., Goodall-Copestake W., Convey P. & Linse K. 2008. Phylum Tardigarda: an “individual” approach. Cladistics 24: 1–18.https://doi.org/10.1111/j.1096-0031.2008.00219.x

Schill, R.O. & Steinbruck G. 2007. Identification and differentiation of Heterotardigrada and Eutardi-grada 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

Schill R.O., Forster F., Dandekar T. & Wolf N. 2010. Using compensatory base change analysis of internal transcribed spacer 2 secondary structures to identify three new species in Paramacrobiotus (Tardigrada). Organisms Diversity & Evolution 10 (4): 287–296. https://doi.org/10.1007/s13127-010-0025-z

Srivathsan A. & Meier R. 2012. On the inappropriate use of Kimura–2–parameter (K2P) divergences in the DNA–barcoding literature. Cladistics 28: 190–194. https://doi.org/10.1111/j.1096-0031.2011.00370.x

Stec D. & Kristensen R.M. 2017. An integrative description of Mesobiotus ethiopicus sp. nov. (Tardi-grada: 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., Smolak R., Kaczmarek Ł. & Michalczyk Ł. 2015. An integrative description of Macrobiotus paulinae sp. nov. (Tardigrada: Eutardigrada: Macrobiotidae: hufelandi group) from Kenya. Zootaxa 4052 (5): 501–526. https://doi.org/10.11646/zootaxa.4052.5.1

Stec D., Morek W., Gąsiorek P., Kaczmarek Ł. & Michalczyk Ł. 2016a. Determinants and taxonomic consequences of extreme egg shell variability in Ramazzottius subanomalus (Biserov, 1985) (Tardigrada). Zootaxa 4208 (2): 176–188. https://doi.org/10.11646/zootaxa.4208.2.5

Stec D., Gąsiorek P., Morek W., Kosztyła P., Zawierucha K., Michno K., Kaczmarek Ł., Prokop Z.M. & Michalczyk Ł. 2016b. 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., Zawierucha K. & Michalczyk Ł. 2017a. An integrative description of Ramazzottius subanomalus (Biserov, 1985) (Tardigrada) from Poland. Zootaxa 4300 (3): 403–420. https://doi.org/10.11646/zootaxa.4300.3.4

Stec D., Morek W., Gąsiorek P., Blagden B. & Michalczyk Ł. 2017b. Description of Macrobiotus scoticus sp. nov. (Tardigrada: Macrobiotidae: hufelandi group) from Scotland by means of integrative taxonomy. Annales Zoologici 67 (2): 181–197. https://doi.org/10.3161/00034541ANZ2017.67.2.001

Stec D., Arakawa K. & Michalczyk Ł. 2018a. 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 (2): e0192210. https://doi.org/10.1371/journal.pone.0192210

Stec D., Roszkowska M., Kaczmarek Ł. & Michalczyk Ł. 2018b. Paramacrobiotus lachowskae, a new species of Tardigrada from Colombia (Eutardigrada: Parachela: Macrobiotidae). New Zealand Journal of Zoology 45 (1): 43–60. https://doi.org/10.1080/03014223.2017.1354896

Stec D., Morek W., Gąsiorek P. & Michalczyk Ł. 2018c. Unmasking hidden species diversity within the Ramazzottius oberhaeuseri complex, with an integrative redescription of the nominal species for the family Ramazzottiidae (Tardigrada: Eutardigrada: Parachela). Systematics and Biodiversity 16 (4): 357–376. https://doi.org/10.1080/14772000.2018.1424267

Stec D., Kristensen R.M. & Michalczyk Ł. 2018d. Integrative taxonomy identifies Macrobiotus papei, a new tardigrade species of the hufelandi complex (Eutardigrada: Macrobiotidae) from the Udzungwa Mountains National Park (Tanzania). Zootaxa 4446 (2): 273–291. https://doi.org/10.11646/zootaxa.4446.2.7

Vaidya G., Lohman D.J. & Meier R. 2011. SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27: 171–180. https://doi.org/10.1111/j.1096-0031.2010.00329.x

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

Wełnicz W., Grohme M.A., Kaczmarek Ł., Schill R.O. & Frohme M. 2011. ITS-2 and 18S rRNA data from Macrobiotus polonicus and Milnesium tardigradum (Eutardigrada, Tardigrada). Journal of Zoological Systematics and Evolutionary Research 49 (S1): 34–39. https://doi.org/10.1111/j.1439-0469.2010.00595.x

Zawierucha K., Kolicka M. & Kaczmarek Ł. 2016. Re-description of the Arctic tardigrade Tenuibiotus voronkovi (Tumanov, 2007) (Eutardigrada; Macrobiotidea), with the first molecular data for the genus. Zootaxa 4196 (4): 498–510. https://doi.org/10.11646/zootaxa.4196.4.2

Zeller C. 2010. Untersuchung der Phylogenie von Tardigraden anhand der Genabschnitte 18S rDNA und Cytochrom c Oxidase Untereinheit 1 (COX I). MSc Thesis, Technische Hochschule Wildau, Germany.

Published
2018-07-24
How to Cite
Stec, D., Krzywański, Łukasz, & Michalczyk, Łukasz. (2018). Integrative description of Macrobiotus canaricus sp. nov. with notes on M. recens (Eutardigrada: Macrobiotidae). European Journal of Taxonomy, (452). https://doi.org/10.5852/ejt.2018.452