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Macrobiotus Noemiae Sp. Nov., a New Tardigrade Species (Macrobiotidae: Hufelandi Group) from Spain

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Macrobiotus Noemiae Sp. Nov., a New Tardigrade Species (Macrobiotidae: Hufelandi Group) from Spain Turkish Journal of Zoology Turk J Zool (2019) 43: 331-348 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1902-5 Macrobiotus noemiae sp. nov., a new tardigrade species (Macrobiotidae: hufelandi group) from Spain 1,2, 1 Milena ROSZKOWSKA *, Łukasz KACZMAREK 1 Department of Animal Taxonomy and Ecology, Adam Mickiewicz University, Poznań, Poland 2 Department of Bioenergetics, Adam Mickiewicz University, Poznań, Poland Received: 14.02.2019 Accepted/Published Online: 14.06.2019 Final Version: 01.07.2019 Abstract: A reexamination of the tardigrade collection from the Museo Nacional de Ciencias Naturales (MNCN) in Madrid was carried out. Specimens from the genera Milnesium, Macrobiotus, and Paramacrobiotus were verified in order to provide their correct identification and 15 taxa were identified. Moreover, a list of corrected species identifications from MNCN is provided. Fourteen specimens and 16 eggs, identified previously as Macrobiotus recens, were attributed to a species new for science. Macrobiotus noemiae sp. nov. is most similar to Mac. naskreckii and Mac. recens but it differs from them by details of egg morphology, mainly by the presence of thin flexible filaments on the tops of egg processes. Key words: Europe, Eutardigrada, systematics, Tardigrada, taxonomy, water bears 1. Introduction not accepted by later authors. In 1993, Bertolani and The phylum Tardigrada consists of about 1300 species Rebecchi redescribed Mac. hufelandi and described (Guidetti and Bertolani, 2005; Degma and Guidetti, three new species of this complex, which resulted in 2007) that inhabit terrestrial, freshwater, and marine 17 species in the group in total. Later, many new taxa environments throughout the world (Ramazzotti and in the hufelandi group were described, and in the most Maucci, 1983 and later translation by Beasley, 1995; recent revision of the group, Kaczmarek and Michalczyk McInnes, 1994; Nelson et al., 2015).1 (2017) listed 47 species attributed to this complex. The tardigrade collection in the Museo Nacional Kaczmarek and Michalczyk (2017) defined the species de Ciencias Naturales (MNCN) in Madrid includes of the hufelandi group based on the presence of cuticular 3785 slides containing in total 19,099 specimens, eggs, pores, two macroplacoids (length sequence: 2 < 1) and a and exuviae. Samples of mosses, lichens, and leaf litter microplacoid in the pharynx, up to three bands of teeth containing tardigrades and their eggs were collected in the oral cavity, Y-shaped claws, egg processes (single- between April 2001 and April 2003 by Noemi Guil López walled) in the shape of inverted chalices (although with and A. Sanchez Ruiz mainly from Spain, but a few samples some exceptions), and a smooth, porous, granulated, or were also collected from France and Belgium. reticulated egg shell. The genus Macrobiotus was described by C.A.S. In this paper, we reexamine tardigrades from the Schultze in 1834 as the first eutardigrade genus. At genera Macrobiotus; Mesobiotus Vecchi, Cesari, Bertolani, present it is the most species-rich genus in the phylum Jönsson, Rebecchi & Guidetti, 2016; Milnesium Doyère, Tardigrada.1 The term “Macrobiotus hufelandi group” was 1840; and Paramacrobiotus Guidetti, Schill, Bertolani, first used by Durante Pasa and Maucci (1979) for species Dandekar & Wolf, 2009 deposited on microscope slides resembling Macrobiotus hufelandi C.A.S Schultze, 1834. in the collection of the Museo Nacional de Ciencias Later, in 1990, Biserov partially revised the hufelandi Naturales, Madrid. Moreover, we provide a description group and proposed the subgenus Macrobiotus for this of a new Macrobiotus species belonging to the hufelandi group of species (Biserov, 1990a, 1990b), but it was group, previously identified as Mac. recens Cuénot, 1932. * Correspondence: [email protected] 1 Degma P, Bertolani R, Guidetti R (2009–2018). Actual checklist of Tardigrada species (v. 34: 30 June 2018), available online at www. tardigrada.modena.unimo.it/miscellanea/Actual%20checklist%20of%20Tardigrada.pdf. 331 This work is licensed under a Creative Commons Attribution 4.0 International License. ROSZKOWSKA and KACZMAREK / Turk J Zool 2. Materials and methods Order: Parachela Schuster, Nelson, Grigarick & 2.1. Microscopy and imaging Christenberry, 1980 According to information from the microscope slides, Superfamily: Macrobiotoidea Thulin, 1928 (in Marley specimens were mounted on microscope slides in Faure’s et al., 2011) medium and secured with a cover slip. Then slides were Family: Macrobiotidae Thulin, 1928 reexamined under an Olympus BX41 phase contrast light Genus: Macrobiotus C.A.S. Schultze, 1834 microscope (PCM) associated with a ARTCAM-300Mi Macrobiotus noemiae sp. nov., Tables 1 and 2, Figures digital camera (Olympus Corporation, Tokyo, Japan). 1–10 All figures were assembled in Corel Photo-Paint 2017. Macrobiotus recens Cuénot, 1932 (Guil, 2002), For deep structures that could not be fully focused in a probably also Macrobiotus recens (in Guil et al., 2009, Guil single photograph, a series of 2–10 images were taken and Sanchez-Moreno, 2013) every ~0.5 µm and then assembled into a single deep- Type material examined: 12 animals, 3 eggs (one with focus image manually in Corel Photo-Paint 2017. embryo) (holotype and 14 paratypes) on microscope slides in Faure’s medium. 2.2. Morphometrics and morphological nomenclature Additional material: 41°00′56.3″N, 3°39′0.6″W, 1040 All measurements are given in micrometers. Structures m a.s.l., Spain, 0.5 km from Gascones, road M-636, next were measured only if their orientation was suitable. to the pond, moss from rock, date 25 Oct. 2001 (2 eggs); Body length was measured from the anterior extremity 41°03′59.3″N, 3°31′9.6″W, 1160 m a.s.l., Spain, on the to the end of the body, excluding the hind legs. The Montejo city limit to La Hiruela, road M-137, leaf litter, types of buccopharyngeal apparatuses and claws were date 25 Oct. 2001 (1 specimen and 7 eggs); 40°50′22.1″N, classified according to Pilato and Binda (2010). All 3°57′16.8″W, 2020 m a.s.l., Spain, Parque Regional de measurements of adults and eggs of Macrobiotus were Peñalara, moss from rock, date 27 May 2001 (1 specimen prepared according to Kaczmarek and Michalczyk (2017). and 3 eggs); 41°06′34.3″N, 3°35′49.6″W, 1280 m a.s.l., Terminology describing the oral cavity armature (OCA) Spain, old road N-I, Dehesa Boyal, Robregordo, leaf litter, follows Michalczyk and Kaczmarek (2003), and OCA date 25 Oct. 2001 (1 egg). morphotypes are given according to Kaczmarek and Michalczyk (2017). The macroplacoid length sequence 3.1.1. Description of the new species was indicated according to Kaczmarek et al. (2014). The Animals (measurements and statistics in Table 1): pt ratio is the ratio of the length of a given structure to the Body transparent after fixation in Faure’s medium, eyes length of the buccal tube expressed as a percentage (Pilato, present in 33% of fixed specimens (Figure 1). Entire 1981). Genus abbreviations follow Perry et al. (2019). cuticle covered with conspicuous small, round pores Morphometric data were handled using the Parachela (0.8–1.1 µm in diameter) distributed randomly. Easily ver. 1.1 template available from the Tardigrada Register visible granulation present on legs I–IV (Figure 5). (Michalczyk and Kaczmarek, 2013). Tardigrade taxonomy Buccopharyngeal apparatus of the Macrobiotus type, follows Bertolani et al. (2014). with ventral lamina and ten peribuccal lamellae (Figures 1 and 2). Mouth anteroventral. Oral cavity armature of 2.3. Comparative material the patagonicus type, with only second and third bands For comparison with the new species, holotype and of teeth visible under light microscope (LM) (Figures 3a paratypes of Mac. naskreckii Bąkowski, Roszkowska, and 3b). The second band of teeth is composed of small Gawlak & Kaczmarek, 2016 from Łukasz Kaczmarek’s granules arranged in several rows, just above the third collection (Department of Animal Taxonomy and Ecology, band of teeth (Figures 3a and 3b, arrow). The third band of Faculty of Biology, Adam Mickiewicz University in Poznań) teeth is composed of three dorsal and three ventral teeth, were used. Moreover, in species identification as well as which appear under LM in the shape of transverse ridges revision of the slides from the MNCN collection, the keys (Figures 3a and 3b, indented arrowhead). Pharyngeal of Morek et al. (2016), Kaczmarek and Michalczyk (2017), bulb spherical with triangular apophyses, two rod- and Kaczmarek et al. (2017) and original descriptions/ shaped macroplacoids, and a triangular microplacoid. redescriptions were also used, i.e. Cuénot (1932), Maucci Macroplacoid length configuration 2 < 1 (Figure 2). The (1979), Ramazzotti and Maucci (1983), Michalczyk et first macroplacoid possesses a central constriction (Figure al. (2006, 2012a, 2012b), Kaczmarek et al. (2012), and 2, empty arrowhead). The second macroplacoid with Ciobanu et al. (2014, 2015). subterminal constriction (Figure 2, filled arrowhead). Claws of the hufelandi type, stout (Figures 4 and 6). 3. Results and discussion Primary branches with distinct accessory points. Lunules 3.1. Taxonomic account of the new species on claws I–III smooth, on claws IV dentate. Thin paired Phylum: Tardigrada Doyère, 1840 cuticular bars under claws I–III present (Figure 5, arrow). Class: Eutardigrada Richters, 1926 Other cuticular thickenings on legs absent. 332 ROSZKOWSKA and KACZMAREK / Turk J Zool Table 1. Measurements (in µm) and pt values of selected morphological
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