Zootaxa, Tardigrada - Biotaxa

Zootaxa 845: 1–46 (2005) www.mapress.com/zootaxa/

ISSN 1175-5326 (print edition)

Copyright © 2005 Magnolia Press

ISSN 1175-5334 (online edition)

ZOOTAXA

Tardigrade taxonomy: an updated check list of the taxa and a list of characters for their identification ROBERTO GUIDETTI & ROBERTO BERTOLANI Department of Animal Biology, University of Modena and Reggio Emilia, Modena, via Campi 213/d, 41100, Modena, Italy. e-mail: [email protected]

Table of contents Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 Table 1. Checklist of Tardigrada . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13 Table 2. Main characters considered in tardigrade taxonomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45

Abstract Since the most recent monograph on Tardigrada by Ramazzotti & Maucci (1983), many changes have been introduced in the systematics of this phylum which has gone through different revisions and has been expanded by several new taxa. Moreover, the number of species is considerably increased (almost doubled to more than 960 species) and new families and genera have been created, while many taxa have been amended. The difficulty in finding a complete, updated list of taxa and the problems with putting together all the newly proposed taxonomic criteria, led us to compile an updated list of tardigrade taxa. This list is supplemented by a series of bibliographic references inherent in the synonymies and/or the amended diagnosis of the taxa occurred after 1983, and a list of the main characters used in the diagnosis of the species. These lists are aimed at helping not only the specialists studying this group, but also researchers interested in biodiversity and those who have to refer to this animal group. Key words: Tardigrada, systematics, check list, taxonomic criteria

Accepted by C.W. Beasley: 12 Jan. 2005; published: 1 Feb. 2005

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Introduction

845 The phylogenetic relationship of tardigrades with respect to other invertebrate phyla has seen different interpretations during the two last centuries. Their position has more recently been evaluated through studies on nucleic acids and/or morphological characters, which support a close phylogenetic relationship between tardigrades and arthropods (Garey et al. 1996; Giribert et al. 1996; Moon & Kim 1996; Min et al. 1998; Regier & Schultz 1998; Edgecombe et al. 2000; Giribert et al. 2000; Schultz & Regier 2000; Giribert & Wheeler 2001; Regier & Shultz 2001). Currently, tardigrades are considered related to Onychophora and Arthropoda (Brusca & Brusca 2003) and according to Zrzavý et al. (1998) and Nielsen (2001) grouped in the taxon Panarthropoda (Onychophora + Tardigrada + Arthropoda). Aguinaldo et al. (1997) propose to include this phylogenetic line within Ecdysozoa, together with other moulting animals (Nematoda, Nematomorpha, Priapulida, and Kinorhyncha). As regards the phylogeny within the phylum, recent morphological and/or molecular studies (Garey et al. 1999; Jørgensen & Kristensen 2004) confirmed the validity of tardigrade classification currently adopted at order level (see below) formally based only on morphological characters. Nonetheless, cladistic and molecular analyses are still rarely applied and the difficulties in interpretation of tardigrade phylogeny are also due to the very scarce number of fossil finds (Cooper 1964; Durante & Maucci 1972; Bertolani & Grimaldi 2000). The only two fossils of ‘true’ tardigrades that were described as new species (both with a single specimen) are: Beorn leggi Cooper, 1964 found in Upper Cretaceous amber ca. 60–80 million years old (Cooper 1964) and Milnesium swolenskyi Bertolani and Grimaldi, 2000 found in Turonian amber 92 million years old (Bertolani & Grimaldi 2000). Even though B. leggi has been attributed to a new family, its interpretation is still controversial, while some current species of Milnesium are differentiated from M. swolenskyi only by morphometric characters, indicating high levels of conservativeness. Recently, four mid Cambrian (ca. 550 million years old) specimens have been attributed to a stem-group of tardigrades (Müller et al. 1995; Mass & Waloszek 2001), relating the origin of tardigrades to the “Cambrian explosion.” The higher taxa subdivision of tardigrades still used, though with minor modifications, is attributed to Marcus (1929, 1936). Marcus divided what he considered the class of Tardigrada into two orders: Heterotardigrada (with 2 suborders: Arthrotardigrada and Echiniscoidea) and Eutardigrada. The identification of these two highest taxa is based mainly on: 1) the presence of a separate gonopore and anus in Heterotardigrada, 2) the presence of a common cloaca and “Malpighian tubules” in Eutardigrada, and 3) different shape and nature between the two taxa of the sclerified structures within the pharynx. In 1937, Rahm discovered Thermozodium esakii Rahm, 1937 that constituted a third order: Mesotardigrada. Some authors do not consider this a valid taxon (e.g., Nelson 2002; Nelson & McInnes 2002).

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GUIDETTI & BERTOLANI

The next comprehensive monograph on tardigrade systematics was the Il Phylum Tardigrada published by Ramazzotti (1962) (for a historical review on the group taxonomy see Ramazzotti & Maucci 1982). In this monograph, tardigrades are considered for the first time as a phylum, with Heterotardigrada, Mesotardigrada and Eutardigrada still as orders. Ramazzotti reported 301 tardigrade species, which in the second edition (Ramazzotti 1972) increased to 417. Pilato (1969a, b) published a new taxonomical scheme for the eutardigrade families and genera based on clear evolutionary principles. Pilato grouped the species using the following criteria: a basal homogeneity in the double-claw structure for the families and homogeneity in claw details and buccal-pharyngeal apparatus morphologies for the genera. A subsequent attempt at a new eutardigrade classification, giving a higher importance to the buccal-pharyngeal apparatus structure with respect to the doubleclaw structure, was proposed by Schuster et al. (1980) but did not receive a large following, even though new taxa and some new characters introduced in that paper are still accepted (for comments on this paper see Pilato 1982). This included the subdivision of the class Eutardigrada into two orders: Apochela (presence of cephalic papillae and claw with separated primary and secondary branches) and Parachela (absence of cephalic papillae and presence of united primary and secondary claw branches). In the class Heterotardigrada, Arthrotardigrada (heterotardigrades with claws or digits directly inserted on the legs) and Echiniscoidea (heterotardigrades with claws inserted on papillae) were also elevated to the level of order. While Arthrotardigrada taxonomy is still quite fluid, the main proposals raised from the 1970’s to present are based on the findings and hypotheses of several authors (for a review see Renaud-Mornant 1982a; see also Renaud-Mornant & Anselme-Moizan 1969; Renaud-Mornant 1974, 1980, 1982a, b, c, 1987, 1989; Kristensen & Hallas 1980; Kristensen & Renaud-Mornant 1983; Pollock 1979, 1983, 1995; Kristensen & Higgins 1984; D’Addabbo Gallo et al. 1986, 1999; Gallo D'Addabbo et al 2000; Grimaldi de Zio 1986; Grimaldi de Zio & D’Addabbo Gallo 1987; de Zio Grimaldi & Villosa-Moreno 1995; Bello & de Zio Grimaldi 1998; de Zio Grimaldi et al. 1998). In Arthrotardigrada, the main criteria to define families and subfamilies are based on the structure of the digits and/or claws (similar to the Pilato’s proposal for Eutardigrada), other than on the characteristics of cephalic appendages and cuticular plates. The main revision of Echiniscoidea systematics is related to the papers by Kristensen and Hallas (1980), Binda and Kristensen (1986) and to the revision based on phylogenetic considerations and cladistic analyses performed on Echiniscidae by Kristensen (1987) and revised by Jørgensen (2000). Marine Heterotardigrada, which include all Arthrotardigrada and a part of Echiniscoidea, have more variable body shapes, compared with the more conservative limno-terrestrial forms of both Heterotardigrada and Eutardigrada. Such diversity is indicated by the fact that 163 marine species of Heterotardigrada are classified in 41 genera and 8 families, whereas 799 limno-terrestrial species belong to only 64 genera and 8 families. The last monograph on the taxonomy of the phylum Tardigrada was written by

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Ramazzotti and Maucci in 1983 (an English translation is available from Dr. Clark Beasley, McMurry University, Abilene, Texas) but after this publication, the taxonomy of the group has gone through several revisions and has been expanded by many new taxa. Moreover, the finding of new taxonomic criteria that were unknown or not considered when the monograph by Ramazzotti and Maucci was published, together with an appreciation of intra-specific variability, has answered several confusing taxonomic problems. These more recent criteria include the use of: 1) the buccal armature structure (Pilato 1972, 1973a, 1974; Schuster et al. 1980), 2) the shape of the apophyses of the buccal tube (Pilato 1987), 3) the pt, ptd, pbf indexes (Pilato 1981; Pilato & Binda 1997/1998; Pilato et al. 2002), 4) sense organs, 5) reproductive systems, 6) dorsal and ventral cuticular plates (Kristensen 1987), 7) the SEM egg details (Toftner et al. 1975; Biserov 1990a, b; Bertolani & Rebecchi 1993), 8) the presence of egg ornamentations (Bertolani 1981; Bertolani & Rebecchi 1993; Bertolani et al. 1996), 9) the spermatozoon ultrastructure (Guidi & Rebecchi 1996; Rebecchi 2001; Rebecchi et al. 2003) and 10) the cuticle ultrastructure (Kristensen & Neuhaus 1999; Guidetti et al. 2000). Other assistance has come from the improvement in available technologies: along with Transmitted Electron Microscopy (TEM) and Scanning Electron Microscopy (SEM), there have been improvements in optical microscopes, digital imaging and computer analyses. Ramazzotti and Maucci (1983) reported 548 species for the phylum; nowadays this number has increased to 959 (see Table 1), slightly less than 100% increase. In addition to a considerable increase in the number of described species, 4 new families, 7 subfamilies, and 55 new genera have been discovered or identified. This period has also seen the transfer of numerous species from one genus to another, while several more species have been synonymized and a considerably high number of taxa have been amended. Actually, the main problems related to tardigrade taxonomy have resulted from: 1) species descriptions using older, now outdated, criteria, 2) different criteria used to described the species, 3) the frequent absence of data indicating the within species variability, and 4) the absence of an updated taxonomic key to the phylum. Further problems may also derive from the difficulty in finding taxonomic references (especially the oldest) and locating the type material. Several genera, mainly the more inclusive (e.g., Echiniscus, Macrobiotus, Isohypsibius), need considerable revision and some of these may prove to be polyphyletic. To begin to alleviate some of the problems mentioned above, an updated list of the taxa used in tardigrade taxonomy is presented (see Table 1). This list is supplemented by a series of bibliographic references inherent in the synonymies and/or the amended diagnoses of the taxa that occurred after 1983, or were not reported by Ramazzotti and Maucci (1983). This list will be useful for specialists of this group and for all researchers interested in biodiversity. The list format (Table 1) follows the rules of the International Code of Zoological Nomenclature — Fourth Edition (1999), with the sequence of taxa to order level following

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the current phylogenetic classification. However, lower taxa within each order (from families to subspecies), are reported in alphabetic order, as the phylogenetic relationships in many cases are still unclear. A list of the main taxonomic characters considered in the species description is presented in Table 2. These characters derive mainly from the analysis (e.g., presence, number, position, morphology, size, symmetry, etc.) of the sclerified structures of animals and eggs such as: cuticle and its appendages, claws and sclerified structures of the buccal-pharyngeal apparatus, egg shell surface and egg processes.

Acknowledgements We would like to thank Prof. Giovanni Pilato, Prof. Maria D’Addabbo Gallo and Jesper G. Hansen for their suggestions, Ms. Barbara Foresti and Dr. Clark Beasley for the English revision of the paper. This work was supported by the University of Modena and Reggio Emilia ex60% MIUR grants.

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hypsibiidae) with remarks on the systematic position of the new genus. Animalia, 14, 65–71. Pilato, G. & Binda, M.G. (1977) Precisazioni e rettifiche alla descrizione di alcune specie di tardigradi (seconda nota). Animalia, 4, 35–51. Pilato, G. & Binda, M.G. (1987) Richtersia, nuovo genere di Macrobiotidae, e nuova definizione di Adorybiotus Maucci e Ramazzotti, 1981 (Eutardigrada). Animalia, 14, 147–152. Pilato, G. & Binda, M.G. (1989) Richtersius, nuovo nome generico in sostituzione di Richtersia Pilato e Binda, 1987 (Eutardigrada). Animalia, 16, 147–148. Pilato, G. & Binda, M.G. (1996) Additional remarks to the description of some genera of eutardigrades. Bollettino della Accademia Gioenia di Scienze Naturali, Catania, 29, 33–40. Pilato, G. & Binda, M.G. (1997/98) A comparison of Diphascon (D.) alpinum Murray, 1906, D. (D.) chilenense Plate, 1889 and D. (D.) pingue Marcus, 1936 (Tardigrada), and description of a new species. Zoologischer Anzeiger, 236, 181–185. Pilato, G. & Binda, M.G. (2003) An opinion on the genus Fujiscon Ito, 1991 (Eutardigrada, Hypsibiidae). Zootaxa, 306, 1–6. Pilato, G., Claxton, S. & Binda, M.G. (1989) Tardigrades from Australia. II. The evaluation of Calohypsibius ornatus (Richters, 1900) caelatus (Marcus, 1928) as valid species and description of Minibiotus fallax n.sp. (Eutardigrada). Animalia, 16, 21–27. Pilato, G., Binda, M.G., Napolitano, A. & Moncada, E. (2000) The specific value of Macrobiotus coronatus De Barros, 1942 and description of two new species of harmsworthi group (Eutardigrada). Bollettino dell’Accademia Gioenia di Scienze Naturali, Catania, 33, 103–120. Pilato, G., Binda, M.G. & Claxton, S. (2002) Itaquascon unguiculum and Itaquascon cambewarrense: two new species of eutardigrades from Australia. New Zealand Journal of Zoology, 29, 87–93. Pilato, G., Binda, M.G. & Lisi, O. (2004) Notes on tardigrades of the Seychelles with the description of three new species. Italian Journal of Zoology, 71, 171–178. Pollock, L.W. (1979) A tabular key to the species of marine Heterotardigrada. Zeszyty Naukowe Uniwersytetu Jagiellonskiego, Prace Zoologiczne, 25, 143–160. Pollock, L.W. (1983) A closer look at some marine Heterotardigrada, II: The morphology and taxonomy of Bathyechiniscus, with a description of B. craticulus n. sp. from the Caribbean. Bulletin of Marine Science, 33 (1), 109–117. Pollock, L.W. (1995) New marine tardigrades from Hawaiian beach sand and phylogeny of the family Halechiniscidae. Invertebrate Biology, 114, 220–235. Rahm, G. (1937) Eine neue Tardigraden-Ordnung aus den heißen Quellen von Unzen, Insel Kyushu, Japan. Zoologischer Anzeiger, 120, 65–71. Ramazzotti, G. (1962) Il Phylum Tardigrada. Memorie dell’Isituto Italiano di Idrobiologia Dott. Marco De Marchi, 14, 1–732. Ramazzotti, G. (1972) Il Phylum Tardigrada. Seconda edizione aggiornata. Memorie dell’Isituto Italiano di Idrobiologia Dott. Marco De Marchi, 28, 1–595. Ramazzotti, G. & Maucci, W. (1982) A history of tardigrade taxonomy. In: D.R. Nelson, (Ed.), Proceedings of the Third International Symposium on the Tardigrada. East Tennessee State University Press, Johnson City, Tennessee, pp. 11–27. Ramazzotti, G. & Maucci, W. (1983) Il Phylum Tardigrada. Terza edizione riveduta e corretta. Memorie dell’Isituto Italiano di Idrobiologia Dott. Marco De Marchi, 41, 1–1012. Rebecchi, L. (2001) The spermatozoon in tardigrades: evolution and relationships with the environment. Zoologischer Anzeiger, 240, 525–533. Rebecchi, L., Guidi A. & Bertolani, R. (2003) The spermatozoon of the Echiniscidae (Tardigrada, Heterotardigrada) and its phylogenetic significance. Zoomorphology, 122, 3–9. Regier, J.C. & Schultz, J.W. (1998) Molecular phylogeny of arthropods and the significance of the Cambrian “Explosion” for Molecular Systematics. American Zoologist, 38, 918–928. Regier, J. C. & Schultz, J.W. (2001) Elongation Factor-2: a useful gene for arthropod phylogenetics.

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Molecular Phylogenetics and Evolution, 20, 136–148. Renaud-Mornant, J.(1974) Une nouvelle famille de Tardigrades marins abyssaux: les Coronarctidae fam. nov. (Heterotardigrada). Comptes Rendus de l'Academie des Sciences. Paris, 278, 3087– 3090. Renaud-Mornant, J. (1980) Description de trois espèces nouvelles du genre Tanarctus RenaudDebyser, 1959, et création de la sous-famille des Tanarctinae, subfam. nov. (Tardigrada, Heterotardigrada). Bulletin du Muséum National d'Histoire Naturelle. 4e Serie, 2, 129–141. Renaud-Mornant, J. (1982a) Species diversity in marine Tardigrada. In: D.R. Nelson (Ed.), Proceedings of the Third International Symposium on the Tardigrada. East Tennessee State University Press, Johnson City, Tennessee, pp. 149–178. Renaud-Mornant, J. (1982b) Tardigrades marins (Arthrotardigrada) du Pacifique Sud. Bulletin du Musee d'Histoire Naturelle de Paris, 3, 799–813. Renaud-Mornant, J.(1982c) Sous-famille et genre nouveaux de Tardigrades marins (Arthrotardigrada). Bulletin du Muséum National d'Histoire Naturelle. 4e Serie, 4, 89–94. Renaud-Mornant, J. (1984) Halechiniscidae (Heterotardigrada) de la campagne Benthedi, canal du Mozambique. Bulletin du Musée d'Histoire Naturelle de Paris, 6, 67–88. Renaud-Mornant, J. (1987) Bathyal and abyssal Coronarctidae (Tardigrada), descriptions of new species and phylogenetical significance. In: R. Bertolani (Ed.), Biology of Tardigrades. Sel. Symp. Monogr. U.Z.I., Vol. 1, Mucchi, Modena, pp. 229–252. Renaud-Mornant, J. (1989) Opydorscus, un nouveau genre d'Orzeliscinae et sa signification phylogénique (Tardigrada, Arthrotardigrada). Bulletin du Museum National d'Histoire Naturelle. 4e Serie, 11, 763–771. Renaud-Mornant, J. & Anselme-Moizan, M.N. (1969) Stades larvaires du tardigrade marin Stygarctus bradypus Schulz et position systématique des Stygarctidae. Bulletin du Muséum National d'Histoire Naturelle. 2e Serie, 41, 883–893. Schultz, J.W. & Regier, J.C. (2000) Phylogenetic analysis of arthropods using two nuclear proteinencoding genes supports a crustacean + hexapod clade. Proceedings of the Royal Society of London, B, Biological Science, 267, 1011–1019. Schuster, R.O. & Toftner, E.C. (1982) Dominican Republic Tardigrada. In: D.R. Nelson (Ed.), Proceedings of the Third International Symposium on the Tardigrada. East Tennessee State University Press, Johnson City, Tennessee, pp. 221–235. Schuster, R.O., Nelson, D.R., Grigarick, A.A. & Christenberry, D. (1980) Systematic criteria of the Eutardigrada. Transactions of the American Microscopical Society, 99, 284–303. Toftner, E.C., Grigarick, A.A., Schuster, R.O. (1975) Analyses of scanning electron microscope images of Macrobiotus eggs. Memorie dell’Isituto Italiano di Idrobiologia Dott. Marco De Marchi, 32, 393–412. Villora-Moreno, S. & de Zio Grimaldi, S. (1993) Redescription and ecology of Batillipes phreaticus Renaud-Debyser, 1959 (Arthrotardigrada, Batillipedidae) in the gulf of Valencia (western mediterranean). Cahiers de Biologie Marine, 34, 387–399. Zrzav&, J., Mihulka, S., Kepka, P., Bezdk, A. & Tietz, D. (1998) Phylogeny of the Metazoa based on morphological and 18S ribosomal DNA evidence. Cladistics, 14, 249–285.

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TABLE 1. Checklist of Tardigrada. The assignment of synonyms and species inquirenda are reported within square parenthesis ‘ [ ] ’ (if the reference is not specified, then the assignments were already reported by Ramazzotti & Maucci 1983). Amendments are reported within arrow parenthesis ‘ < > ’. Comments are reported within brace parenthesis ‘ { } ’. The species written in bold characters are the genus type species. TARDIGRADA HETEROTARDIGRADA Marcus, 1927 ARTHROTARDIGRADA Marcus, 1927 Batillipedidae Ramazzotti, 1962 [Discopodidae Marcus, 1934]

18



ZOOTAXA

Renaudarctidae Kristensen & Higgins, 1984

845

Renaudarctus Kristensen & Higgins, 1984 Renaudarctus psammocryptus Kristensen & Higgins, 1984 Stygarctidae Schulz, 1951