A Comprehensive and Integrative Re-Description of Synchaeta Oblonga and Its Relationship to Synchaeta Tremula, Synchaeta Rufina

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A Comprehensive and Integrative Re-Description of Synchaeta Oblonga and Its Relationship to Synchaeta Tremula, Synchaeta Rufina Organisms Diversity & Evolution (2018) 18:407–423 https://doi.org/10.1007/s13127-018-0380-8 ORIGINAL ARTICLE A comprehensive and integrative re-description of Synchaeta oblonga and its relationship to Synchaeta tremula, Synchaeta rufina and Synchaeta littoralis (Rotifera: Monogononta) Tanja Wilke1 & Wilko H. Ahlrichs1 & Olaf R. P. Bininda-Emonds1 Received: 27 June 2018 /Accepted: 20 September 2018 /Published online: 11 October 2018 # Gesellschaft für Biologische Systematik 2018 Abstract A comprehensive re-description of the monogonont rotifer Synchaeta oblonga Ehrenberg, 1832 is presented with the aim of creating a specific and robust suite of characters to identify this species that takes account of its morphological intraspecific variability. To accomplish this, we used an integrative approach that combined morphological data of the habitus and trophi (light and scanning electron microscopy) together with ecological and molecular data to generate a data set that clearly delineates S. oblonga from the morphologically similar Synchaeta tremula (Müller, 1786) with which it is often confused. In addition, by comparing S. oblonga to all remaining members of the genus Synchaeta, we found that the literature descriptions of Synchaeta rufina Kutikova and Vasiljeva, 1982, a Lake Baikal endemic species, and Synchaeta littoralis Rousselet, 1902, a species whose taxonomic status with respect to S. oblonga had already been called into question, to both lie entirely within the range of intraspecific morphological variability present in S. oblonga. Thus, we conclude that S. oblonga can be clearly demarcated from S. tremula, but that no unambiguous morphological differences exist to delineate it from either S. rufina or S. littoralis.Because our molecular data indicate S. oblonga to be a single species despite the morphological intraspecific variability that is present, we recommend that thorough re-examinations of the taxonomic statuses of both S. rufina and S. littoralis should be performed on topotypes sampled from their type localities (Lake Baikal, Russia and Dundee, Scotland, respectively). Keywords Rotifera . Morphology . Trophi . Species delimitation . Synonymy . Intraspecific variability Introduction (Stemberger and Gilbert 1985), often to the point of compris- ing most of the metazooplankton biomass (Arndt et al. 1990). Rotifers are microscopic, aquatic animals that occur in nearly Synchaetid rotifers were therefore among the first rotifers to any habitat where water is available (Fontaneto and De Smet have been observed by the early microscopists (Rousselet 2015), but they are particularly abundant in freshwater (Koste 1902), with Synchaeta oblonga Ehrenberg, 1832 being one 1978; Fontaneto et al. 2006) where they represent one of the of the first known members of this genus together with main groups of Metazoa (Segers 2004). Because of their rapid Synchaeta tremula (Müller, 1786) and Synchaeta pectinata turnover rates and high population densities, their importance Ehrenberg, 1832. in aquatic food webs is undisputed (Segers 2004;Fontaneto Synchaeta oblonga is considered to be a cosmopolitan spe- and De Smet 2015), with species of the genus Synchaeta typ- cies (Hollowday 2002) and, although it is omnipresent in nu- ically being a dominant form within the rotifer community merous ecological studies (e.g. Duggan et al. 2002; Zimmermann-Timm et al. 2007;Zengetal.2017), its mor- phological descriptions in the literature often show large dis- * Tanja Wilke crepancies to one another (see Hollowday 2002). This is [email protected] thought to derive from natural intraspecific variability (Koste 1978; Shiel and Koste 1993) and/or from the absence of any delimiting, species-specific characters for S. oblonga, such 1 AG Systematik und Evolutionsbiologie, Institut für Biologie und Umweltwissenschaften (IBU), Carl von Ossietzky Universität that the resulting potential morphological overlap with other Oldenburg, 26111 Oldenburg, Germany Synchaeta species can easily lead to a misidentification 408 Wilke T. et al. (Donner 1959). For example, S. oblonga is often confused were measured using a WTW Multi 340 measuring instru- with the morphologically similar and likewise common S. ment (WTW, Weilheim, Germany). tremula in the literature (e.g. Voigt 1956–1957; Donner 1959; Obertegger et al. 2006) and both species are often clus- Species identification and examination of the habitus tered together by several authors (Synchaeta gr. tremula- using light microscopy oblonga sensu Ruttner-Kolisko 1972; Obertegger et al. 2006; Dokulil and Herzig 2009; Wærvågen and Andersen Individuals were identified to species level by consulting the 2017). Although such a clustering might represent a conser- morphological descriptions of the habitus and the trophi of vative or practical solution, it could imply a close evolutionary Synchaeta species found in Voigt (1956–1957), Koste relationship between these species that might not exist and/or (1978) and Hollowday (2002). To identify specimens of S. call their status as distinct species even further into question oblonga, particular emphasis was placed on those characters (cf. Ruttner-Kolisko 1972). that were invariable between these sources for this species. Therefore, following the suggestion of Obertegger et al. For morphological investigations by light microscopy (LM), (2006), we seek to clarify the taxonomic status of S. oblonga a total of 35–40 mature, live individuals of S. oblonga were with respect to S. tremula based on comprehensive morpho- analysed. Single specimens were initially sedated with car- logical and molecular analyses of reliably identified speci- bonated water and kept in place through the slight pressure mens of both species. In particular, we investigated numerous of a cover glass. Examinations using differential interference live and preserved individuals of S. oblonga with the goal of contrast were performed using a Leica DMLB microscope, generating a robust suite of characters (mostly comprising the and each individual was digitally photographed using a habitus and trophi) that could delineate it from all remaining Canon EOS 5D Mark II camera. Photo series of the various members of Synchaeta and from S. tremula in particular (with layers of each specimen were condensed to a single image comparable data for the latter species coming primarily from using the software Picolay (www.picolay.de). Wilke et al. (2017)). In so doing, we took special account of the apparent intraspecific variability in S. oblonga (as sug- Examination of trophi and habitus using scanning gested by Donner 1959) and likewise attempted to clarify electron microscopy the many ambiguous morphological statements about it from the literature. The molecular analyses to verify the distinctive- Additional 30–35 mature individuals of S. oblonga were used ness of S. oblonga with respect to S. tremula are highlighted for scanning electron microscopy (SEM) examinations of ei- by the first molecular data obtained specifically for S. ther the habitus or the trophi. To examine the isolated trophi, the oblonga. Finally, the comparison to all remaining species of surrounding tissue of the specimen was dissolved with sodium Synchaeta is important to reveal potential cases of synonymy, dodecyl sulfate (SDS) and dithiothreitol (DTT, AppliChem, especially with respect to more poorly known species, as we Darmstadt, Germany) following the protocol of Kleinow et recently showed for Synchaeta jollyae Shiel and Koste, 1993 al. (1990). Thereafter, single specimens were transferred into and Synchaeta stylata Wierzejski, 1893 (Wilke et al. 2018). In a droplet of dissolving agent (0.1 g DTT in a 5-ml stock solu- the current context, we could find no convincing differences tion of 5.2 g SDS + 0.24 g NH4HCO3 in 100 ml Aqua Dest) for between the suite of characters we used to delineate S. about 15 min before being washed with distilled water. For oblonga and the literature descriptions of either Synchaeta investigations of the habitus, whole individuals were initially rufina Kutikova and Vasiljeva, 1982 or Synchaeta littoralis sedated with carbonated water before being euthanized with Rousselet, 1902, thereby highlighting the need for a taxonom- 1% OsO4 buffered in 0.1 M NaCa cacodylate buffer and sub- ic re-examination of these two latter species. sequently fixed with 240 mOsmol picric acid-formaldehyde (Melone and Ricci 1995). Both habitus and the fragile trophi samples were then dehydrated using an ascending, graded eth- Material and methods anol series followed by critical-point drying (to avoid any dam- age or deformations caused by changes in surface tension dur- Study site and sampling ing normal drying) before being attached onto an SEM stub and coated with a 15-nm-thick layer of gold palladium. All samples Samples were taken monthly between May 2015 and May were examined on a Hitachi S-3200N SEM. 2017 at the Schlossteich in Oldenburg, northwest Lower Saxony, Germany (ST; N 53.1603°, E 8.1195) using a Morphometric analysis and habitus drawing plankton net with a mesh size of 55 μm. The Schlossteich is a permanent freshwater pond with constant Measurements of the body were made from the LM digital water in- and outflows. At each sampling event, water images using the software ImageJ 1.46r (http://imagej.nih. temperature, oxygen concentration, conductivity and pH gov/ij/). The total body length was measured from the central A comprehensive and integrative re-description of Synchaeta oblonga and its relationship to... 409 apex of
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