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Integrative Descriptions of Two New Macrobiotidae Species (Tardigrada: Eutardigrada: Macrobiotoidea) from French Guiana and Malaysian Borneo

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Integrative Descriptions of Two New Macrobiotidae Species (Tardigrada: Eutardigrada: Macrobiotoidea) from French Guiana and Malaysian Borneo Zoological Studies 59:23 (2020) doi:10.6620/ZS.2020.59-23 Open Access Integrative Descriptions of Two New Macrobiotidae Species (Tardigrada: Eutardigrada: Macrobiotoidea) from French Guiana and Malaysian Borneo Daniel Stec1,*, Magdalena Dudziak1, and Łukasz Michalczyk1 1Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387 Kraków, Poland. *Correspondence: E-mail: [email protected] (Stec) E-mail: [email protected] (Dudziak); [email protected] (Michalczyk) Received 27 March 2020 / Accepted 12 May 2020 / Published 2 July 2020 Communicated by Benny K.K. Chan In this paper we describe two new tardigrade species, one representing the Macrobiotus hufelandi complex and the other from the Paramacrobiotus richtersi complex. The descriptions are based on a detailed morphological examination under light and scanning electron microscopy and analysis of four genetic markers (18S rRNA, 28S rRNA, ITS-2 and COI). Macrobiotus crustulus sp. nov. from French Guiana is the most similar to Macrobiotus martini Bartels, Pilato, Lisi and Nelson, 2009, Macrobiotus santoroi Pilato and D'Urso, 1976, but differs from them mainly by having the lissostomus type of the oral cavity armature (teeth not visible under light microscopy) and well-developed, convex terminal discs of egg processes covered with evident granulation. Paramacrobiotus filipi sp. nov. from the Malaysian part of Borneo is the most similar to Paramacrobiotus alekseevi (Tumanov, 2005), but differs from it primarily by the presence of body granulation visible under light microscopy as well as sculptured and porous areoles around egg processes. Key words: Biodiversity, DNA barcodes, New species, Species complex, Taxonomy. BACKGROUND the last few decades, there are still regions of the world where these animals have never been studied. One such Tardigrades are a phylum of ubiquitous places is French Guiana, an overseas department of the microinvertebrates that inhabit marine and limno- French Republic located in the northern Atlantic coast of terrestrial environments throughout the world (Nelson South America. Another part of the globe with weakly et al. 2015). Currently, there are nearly 1300 formally investigated tardigrade fauna is Malaysia where the only recognised tardigrade species (Guidetti and Bertolani records come from its eastern part, Malaysian, Borneo, 2005; Degma and Guidetti 2007; Degma et al. 2009– but with no reports from the peninsular part of the 2019). Although the great majority of species have been country. However, the Bornean tardigrade fauna is also described classically, the number of taxa described very poorly known, as only four species from the island under the integrative taxonomy framework is constantly have been recorded so far: Famelobiotus scalicii Pilato, increasing (e.g., Surmacz et al. 2019; Bochnak et Binda and Lisi, 2004, Bryodelphax arenosus Gąsiorek, al. 2020; Kayastha et al. 2020). Although studies on 2018, Echiniscus masculinus Gąsiorek, Vončina and tardigrades have been conducted for more than two Michalczyk, 2020 and Insulobius orientalis Gąsiorek centuries, and have been particularly prevalent during and Michalczyk, 2020. Citation: Stec D, Dudziak M, Michalczyk Ł. 2020. Integrative descriptions of two new Macrobiotidae species (Tardigrada: Eutardigrada: Macrobiotoidea) from French Guiana and Malaysian Borneo. Zool Stud 59:23. doi:10.6620/ZS.2020.59-23. © 2020 Academia Sinica, Taiwan 1 Zoological Studies 59:23 (2020) page 2 of 25 In this paper, we provide integrative descriptions of after mounting (Coughlan et al. 2019). In order to obtain two new Macrobiotidae species, Macrobiotus crustulus clean and extended specimens for SEM, tardigrades sp. nov. from French Guiana and Paramacrobiotus were processed according to the protocol by Stec et al. filipi sp. nov. from the Malaysian part of Borneo. In (2015). Specimens were examined under high vacuum addition, we also present new photomicrographs of the in a Versa 3D DualBeam Scanning Electron Microscope types of Paramacrobiotus alekseevi (Tumanov, 2005) (SEM) at the ATOMIN facility of the Jagiellonian and amend its description. The detailed morphological University, Kraków, Poland. All figures were assembled and morphometric data were obtained using light in Corel Photo-Paint X6, ver. 16.4.1.1281. For structures contrast and scanning electron microscopy. These data that could not be satisfactorily focused in a single PCM were further associated with DNA sequences of four photograph, a stack of 2–6 images were taken with an genetic markers that are standard in modern tardigrade equidistance of ca. 0.2 μm and assembled manually into taxonomy (the nuclear 18S rRNA, 28S rRNA, and ITS- a single deep-focus image in Corel Photo-Paint. 2, and the mitochondrial COI). Morphometrics and morphological nomenclature MATERIALS AND METHODS All measurements are given in micrometres (μm). The moss sample containing Macrobiotus Sample size was adjusted following recommendations crustulus sp. nov. was collected by Witold Morek and by Stec et al. (2016). Structures were measured only Bartłomiej Surmacz on 2 April 2019 from a tree trunk if their orientation was suitable. Body length was in the primeval tropical rainforest in the vicinity of measured from the anterior extremity to the end of the Patawa, French Guiana, South America (4°33'58.2"N, body, excluding the hind legs. The terminology used to 52°9'12.36"W; 268 m asl). The epiphyllous moss describe oral cavity armature and egg shell morphology sample containing Paramacrobiotus filipi sp. nov. was follows Michalczyk and Kaczmarek (2003) and collected by Piotr Gąsiorek on 27 July 2016 from the Kaczmarek and Michalczyk (2017). The type of buccal leaf of a tree in the primary tropical forest, Gunung apparatus and claws are given according to Pilato and Mulu, Sarawak, Borneo, Malaysia, Asia (4°02'N; Binda (2010). Macroplacoid length sequence is given 114°49'E; 100 m asl). according to Kaczmarek et al. (2014). Buccal tube Both samples were examined for tardigrades using length and the level of the stylet support insertion point the protocol by Dastych (1980) with modifications were measured according to Pilato (1981). The pt index described in detail in Stec et al. (2015). A total of 55 is the ratio of the length of a given structure to the length and 28 animals as well as 45 and 15 eggs of the two of the buccal tube, expressed as a percentage (Pilato new species were extracted from the South American 1981). All other measurements and nomenclature follow and Asian samples, respectively. In order to perform Kaczmarek and Michalczyk (2017). Morphometric data integrative taxonomic descriptions, the isolated animals were handled using the “Parachela” ver. 1.7 template and eggs were split into three groups for specific available from the Tardigrada Register (Michalczyk analyses: morphological analysis with phase contrast and Kaczmarek 2013). Raw morphometric data for light microscopy (PCM), morphological analysis each analysed species are provided as supplementary with scanning electron microscopy (SEM), and DNA materials (Table S1 and Table S2) and are deposited sequencing (for details please see sections “Material in the Tardigrada Register under www.tardigrada.net/ examined” provided below for each description). register/0068.htm (M. crustulus sp. nov.) and www. tardigrada.net/register/0069.htm (P. filipi sp. nov.). Microscopy and imaging Tardigrade taxonomy follows Bertolani et al. (2014a). Specimens for light microscopy were mounted on Comparative material microscope slides in a small drop of Hoyer’s medium and secured with a cover slip, following the protocol First, to test whether our species had previously by Morek et al. (2016). Slides were examined under been described, we used dichotomous keys for the an Olympus BX53 light microscopy, associated with Macrobiotus hufelandi complex (Kaczmarek and an Olympus DP74 digital camera. Immediately after Michalczyk 2017) and for the genus Paramacrobiotus mounting the specimens in the medium, slides where (Kaczmarek et al. 2017). As they did not key to a also checked under PCM for the presence of males and recognised species, the specimens were compared with females in the studied population as the spermatozoa the original descriptions of the species most similar in testis and spermathecae are visible for several hours to them: Macrobiotus martini Bartels, Pilato, Lisi and © 2020 Academia Sinica, Taiwan Zoological Studies 59:23 (2020) page 3 of 25 Nelson, 2009, Macrobiotus santoroi Pilato and D'Urso, rRNA, nDNA), large ribosome subunit (28S rRNA, 1976 and Paramacrobiotus alekseevi (Tumanov, 2005). nDNA), internal transcribed spacer (ITS-2, nDNA), Additionally, we used two slides containing a paratype and cytochrome oxidase subunit I (COI, mtDNA). All and six eggs of P. alekseevi and new microphotographs fragments were amplified and sequenced according to of paratypes, which were kindly sent to us by Denis the protocols described in Stec et al. (2020c); primers Tumanov (Saint-Petersburg State University, Russia). used in this study are listed in table 1. Sequencing products were read with the ABI 3130xl sequencer at Genotyping the Molecular Ecology Lab, Institute of Environmental Sciences of the Jagiellonian University, Kraków, Individual DNA extractions were made from Poland. Sequences were processed in BioEdit ver. 7.2.5 eight specimens (four specimens per each new species) (Hall 1999) and submitted to GenBank. following protocol by Casquet et al. (2012) with modification
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