Abstract
Species of the Macrobiotus hufelandi group are one of the most often recorded tardigrades throughout the globe. For over a century M. hufelandi has been considered cosmopolitan but in recent decades numerous species of similar morphologies have been described from various continents, which suggests that what was originally defined as a single taxon is, in fact, a complex of species. The definition of the hufelandi group is subject to a long-standing discussion and in this paper we propose a refined set of characters that are hoped to elucidate the taxonomic status of the group. In order to aid interspecific comparisons, we also propose a unified nomenclature for the crucial morphological traits and clar
References
Barros, R. de (1942) Tardigrados de Estado de Sao Paulo, Brasil. II. Gênero Macrobiotus. Revista Brasileira de Biologia, 2, 373–386.
Bartels, P., Pilato, G., Lisi, O. & Nelson, D.R. (2009) Macrobiotus (Eutardigrada, Macrobiotidae) from the Great Smoky Mountains National Park, Tennessee/North Carolina, USA (North America): two new species and six new records. Zootaxa, 2022, 45–57.
Bąkowski, M., Roszkowska, M., Gawlak, M. & Kaczmarek, Ł. (2016) Macrobiotus naskreckii sp. nov., a new tardigrade (Eutardigrada: Macrobiotidae) of the hufelandi group from Mozambique. Annales Zoologici, 66 (2), 155–164.
https://doi.org/10.3161/00034541ANZ2016.66.2.001
Beasley, C.W. (1995) The phylum Tardigrada. Third Edition by G. Ramazzotti and W. Maucci, English Translation. Published by the translator Clark Beasley, Abilene, USA, pp 1014.
Bertolani, R. & Biserov, V.I. (1996) Leg and claw adaptations in soil tardigrades, with erection of two new genera of Eutardigrada, Macrobiotidae: Pseudohexapodibius and Xerobiotus. Invertebrate Biology, 115, 299–304.
https://doi.org/10.2307/3227019
Bertolani, R. & Pilato, G. (1988) Struttura delle unghie nei Macrobiotidae e descrizione di Murrayon n. gen. (Eutardigrada). Animalia, 15, 17–24.
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., Guidi, A. & Rebecchi, L. (1996) Tardigradi della Sardegna e di alcune piccole isole circum-sarde. Biogeographia, 18, 229–247.
https://doi.org/10.21426/B618110456Bertolani, R., Rebecchi, L. & Cesari M. (2010) A model study for tardigrade identification. In: Nimis, P.L. & Vignes Lebbe, R. (Eds.), Tools for Identifying Biodiversity: Progress and Problems. EUT, Trieste, pp. 333–339.
Bertolani, R., Biserov, V., Rebecchi, L. & Cesari, M. (2011a) 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., Rebecchi, L., Giovannini, I. & Cesari, M. (2011b) 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., 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. (1972) Tardigradi muscicoli di Sicilia (IV Nota). Bollettino delle sedute della Accademia Gioenia di Scienze Naturali in Catania, Series 4, 11, 47–60.
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. Bollettino Accademia Gioenia Science Naturali in Catania, 34 (360), 101–111.
Biserov, V.I. (1990a) On the revision of the genus Macrobiotus. The subgenus Macrobiotus s. str.: 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. str. is a new systematic status of the hufelandi group (Tardigrada, Macrobiotidae). Communication, 2. Zoologicheskii Zhurnal, 69, 38–50.
Biserov, V.I. (1990c) New species of Tardigrada in the USSR fauna. Zoologicheskii Zhurnal, 69, 17–25.
Biserov, V.I. (1994) Some tardigrades from the Seychelles with description of three new species. Tropical Zoology, 7, 181–189.
https://doi.org/10.1080/03946975.1994.10539250
Biserov, V., Pilato, G. & Lisi, O. (2011) Macrobiotus trunovae sp.n., a new species of tardigrade from Russia. Invertebrate Zoology, 8 (1), 57–62.
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.
Cuénot, L. (1932) Tardigrades. In: Lechevalier, P. (Ed.), Faune de France, 24, pp. 1–96.
Dastych, H. (1978) Parhexapodibius xerophilus sp. nov., a new species of Tardigrada from Poland. Bulletin de L'Academie Polonaise des Sciences Série des Sciences Biologiques, 26, 479–481.
Dastych, H. (2002) A new species of the genus Macrobiotus Schultze, 1834 from Iles Kerguélen, in the sub-Antarctic (Tardigrada). Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut, 99, 11–27.
Dastych, H. (2005) Macrobiotus ramoli sp. nov., a new tardigrade species from the nival zone of the Ötztal Alps, Austria (Tardigrada). Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut, 102, 21–35.
Dastych, H. & Alberti, G. (1990) Redescription of Macrobiotus xerophilus (Dastych, 1978) comb. nov., with some phylogenetic notes (Tardigrada, Macrobiotidae). Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut, 87, 157–169.
Durante Pasa, M.V. & Maucci, W. (1979) Tardigradi muscicoli della Grecia. Zeszyty Naukowe Uniwersytetu Jagiellońskiego, Prace Zoologiczne, 25, 19–45.
Eichorn, J.C. (1775) Beyträge zur Natur-Geschicte der kleinsten Wasser Thierchen (8 Kupfer-Tafeln, p. 74, tab. 7, fig. E). Der Wasser-Bar. Danzig.
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.
Fontoura, P., Rubal, M. & Veiga, P. (2017) Two new species of Tardigrada (Eutardigrada: Ramazzottiidae, Macrobiotidae) from the supralittoral zone of the Atlantic Iberian Peninsula rocky shores. Zootaxa, 4263 (3), 450–466.
Gąsiorek, P., Stec, D., Morek, W., Zawierucha, K., Kaczmarek, Ł. & Michalczyk, Ł. (2016) An integrative revision of Mesocrista Pilato, 1987 (Tardigrada: Eutardigrada: Hypsibiidae). Journal of Natural History, 50 (45–46), 2803–2828.
https://doi.org/10.1080/00222933.2016.1234654Guidetti, R. (1998) Two new species of Macrobiotidae (Tardigrada: Eutardigrada) from the United States of America, and some taxonomic considerations of the genus Murrayon. Proceedings of the Biological Society of Washington, 111, 663–673.
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., 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
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., Rebecchi, L., Bertolani, R., Jönsson, K.I., Kristensen, R.M. & Cesari, M. (2016) Morphological and molecular analyses on Richtersius (Eutardigrada) diversity reveal its new systematic position and lead to the establishment of a new genus and a new family within Macrobiotoidea. Zoological Journal of the Linnean Society, 178 (4), 834–845.
https://dx.doi.org/10.1111/zoj.12428
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.xHorning, D., Schuster, R. & Grigarick, A. (1978) Tardigrada of New Zealand. New Zealand Journal of Zoology 5, 185–280.
https://doi.org/10.1080/03014223.1978.10428316
Iharos, G. (1966) Beiträge zur Kenntnis der Tardigraden-Fauna Österreichs. Acta Zoologica Hungaricae, 12, 123–127.
Iharos, G. (1973) Neuere Daten zur Kenntnis der Tardigraden-Fauna von Neuguinea. Opuscula Zoologica, Budapest, 11, 65–73.
Jonckheere A.R. (1954) A distribution-free k-sample test against ordered alternatives. Biometrika, 41, 133–145.
https://doi.org/10.1093/biomet/41.1-2.133Kaczmarek, Ł. & Michalczyk, Ł. (2004) New records of Tardigrada from Cyprus with a description of the new species Macrobiotus marlenae (hufelandi group) (Eutardigrada: Macrobiotidae). Genus, 15, 141–152.
Kaczmarek, Ł. & Michalczyk, Ł. (2006) Redescription of Macrobiotus tridigitus Schuster, 1983 and erection of a new genus of Tardigrada (Eutardigrada, Macrobiotidae). Journal of Natural History, 40 (19–20), 1223–1229.
https://doi.org/10.1080/00222930600844443
Kaczmarek, Ł. & Michalczyk, Ł. (2017) 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 (1), 079–100.
https://doi.org/10.11646/zootaxa.4363.1.3Kaczmarek, 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
Maucci, W. (1954) Tardigradi nuovi della fauna Italiana. Atti della Societa Italiana di Scienze Naturali e del Museo Civico di Storia Naturale di Milano, 93, 576–585.
Maucci, W. (1988) Tardigrada from Patagonia (Southern South America) with description of three new species. Revista Chilena de Entomologia, 16, 5–13.
Maucci, W. (1993) Prime notizie su Tardigradi "terrestri" del Madagascar con descrizione di tre specie nuove. Bollettino del Museo Civico di Storia Naturale di Verona, 17, 381–392.
Maucci, W. & Ramazzotti, G. (1981) Adorybiotus gen. nov.: nouva posizione sistematica per Macrobiotus granulatus Richters, 1903 e per Macrobiotus coronifer Richters, 1903 (Tardigrada, Macrobiotidae). Memorie dell'Istituto italiano di idrobiologia, Pallanza, 39, 153–159.
Meyer, H.A. (2012) A new water bear, Minibiotus julianae, from the Caribbean Island of Dominica (Tardigrada: Eutardigrada: Parachela: Macrobiotidae). Proceedings of the Biological Society of Washington, 125 (1), 54–60.
https://doi.org/10.2988/11-15.1
Meyer, H.A. & Domingue, M.D. (2011) Minibiotus acadianus (Eutardigrada: Macrobiotidae), a new species of Tardigrada from southern Louisiana, USA. Western North American Naturalist, 71 (1), 38–43.
https://doi.org/10.3398/064.071.0106
Meyer, H.A., Domingue, M.N. & Hinton, J.G. (2014) Tardigrada of the West Gulf Coastal Plain, with descriptions of two new species from Louisiana. Southeastern Naturalist, 13 (5), 117–130.
https://doi.org/10.1656/058.013.s511
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, (Supplement 1), 175–181.
https://doi.org/10.4081/jlimnol.2013.s1.e22
Pamilo, P. & Nei, M. (1988) Relationships between gene trees and species trees. Molecular Biology and Evolution, 5 (5), 568–583.
Pilato, G. (1969) Evoluzione e nuova sistemazione degli Eutardigrada. Bolletino di Zoologia, 36, 327–345.
https://doi.org/10.1080/11250006909436925
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), 1–7.
https://doi.org/10.11646/zootaxa.638.1.1Pilato, G. & Binda, M.G. (1983) Descrizione du una nuova specie di Eutardigrado d`Australia Macrobiotus joannae n. sp. Animalia, 10, 262–272.
Pilato, G. & Binda, M.G. (1989) Richtersius, nuove nome generico in sostituzione di Richtersia Pilato e Binda 1987 (Eutardigrada). Animalia, 16, 147–148.
Pilato, G. & D`Urso, V. (1976) Contributo alla conoscenza dei Tardigradi d`Australia. Animalia, 3, 135–145.
Pilato, G., Binda, M.G. & Azzaro, M. (1990) Tardigradi di Terra del Fuoco e Magallanes. III. Macrobiotus punctillus, nuova specie di Macrobiotidae del gruppo hufelandi. Animalia, 17, 123–129.
Pilato, G., Binda, M.G. & Catanzaro, R. (1991) Remarks on some tardigrades of the African fauna with the description of three new species of Macrobiotus Schultze 1834. Tropical Zoology, 4, 167–178.
https://doi.org/10.1080/03946975.1991.10539487
Pilato, G., Binda, M.G. & Lisi, O. (2006) Eutardigrada from New Zealand, with descriptions of two new species. New Zealand Journal of Zoology, 33, 49–63.
https://doi.org/10.1080/03014223.2006.9518430Pilato, G., Kaczmarek, Ł., Michalczyk, Ł. & Lisi, O. (2003) Macrobiotus polonicus, a new species of Tardigrada from Poland (Eutardigrada: Macrobiotidae, "hufelandi group"). Zootaxa, 258 (1), 1–8.
https://doi.org/10.11646/zootaxa.258.1.1Pilato, G. & Lisi, O. (2009) Description of three new species of Tardigrada from the Seychelles. Zootaxa 2005, 24–34.
Pilato, G. & Lisi, O. (2010) Tenuibiotus, a new genus of Macrobiotidae (Eutardigrada). Zootaxa, 2761, 34–40.
Pilato, G., Kiosya, Y., Lisi, O. & Sabella, G. (2012) New records of Eutardigrada from Belarus with the description of three new species. Zootaxa, 3179, 39–60.
Poprawa, I., Schlechte-Wełnicz, W. & Hyra, M. (2015) Ovary organization and oogenesis in the tardigrade Macrobiotus polonicus Pilato, Kaczmarek, Michalczyk & Lisi, 2003 (Eutardigrada, Macrobiotidae): ultrastructural and histochemical analysis. Protoplasma, 252, 857–865.
https://doi.org/10.1007/s00709-014-0725-x
Ramazzotti, G. & Maucci, W. (1983) Il Phylum Tardigrada. Memorie dell'Istituto italiano di idrobiologia, Pallanza, 41, 1–1012.
Richters, F. (1903) Arktische Tardigraden. Fauna Arctica, 3, 494–508.
Richters, F. (1908) Moosbewohner. Wissenschaftliche Ergebnisse der Schwedischen Südpolar-Expedition (1901–1903) Stockholm, 6, 1–16.
Roszkowska, M., Stec, D., Ciobanu, D.A. & Kaczmarek, Ł. (2016) Tardigrades from Nahuel Huapi National Park (Argentina, South America) with descriptions of two new Macrobiotidae species. Zootaxa, 4105 (3), 243–260.
https://doi.org/10.11646/zootaxa.4105.3.2Roszkowska, M., Ostrowska, M., Stec, D., Janko, K. & Kaczmarek, Ł. (2017) Macrobiotus polypiformis, a new tardigrade (Macrobiotidae; hufelandi group) from the Ecuadorian Pacific coast, remarks on the claw abnormalities and the taxonomic status of Mesobiotus armatus (Pilato & Binda, 1996). European Journal of Taxonomy, 327, 1–19.
Schultze, C.A.S. (1834) Macrobiotus Hufelandii animal e crustaceorum classe novum, reviviscendi post diuturnam asphixiam et aridiatem potens. Berolini Apud Carolum Curths, 1834, 1–8.
Schuster, R.O., Nelson, D.R., Grigarick, A.A. & Christenberry, D. (1980) Systematic criteria of Eutardigrada. Transactions of the American Microscopical Society, 99, 284–303.
https://doi.org/10.2307/3226004
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., Gąsiorek, P., Morek, W., Kaczmarek, Ł. & Michalczyk, Ł. (2016) 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., Morek, W., Gąsiorek, P., Blagden, B. & Michalczyk, Ł. (2017) Description of Macrobiotus scoticus sp. nov. (Tardigrada: Macrobiotidae: hufelandi group) from Scotland by means of integrative taxonomy. Annales Zoologici, 67, 181–197.
https://doi.org/10.3161/00034541ANZ2017.67.2.001Stec, 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
Terpstra, T.J. (1952) The asymptotic normality and consistency of Kendall's test against trend, when ties are present in one ranking. Indagationes Mathematicae, 14, 327–333.
https://doi.org/10.1016/S1385-7258(52)50043-XVecchi, M., Cesari, M., Bertolani, R., Jönsson, I.K., Rebecchi, L. & Guidetti, R. (2017) 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