Systematic Re-Structure and New Species of Sphaerodoridae (Annelida) After Morphological Revision and Molecular Phylogenetic Analyses of the North East Atlantic Fauna

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Systematic Re-Structure and New Species of Sphaerodoridae (Annelida) After Morphological Revision and Molecular Phylogenetic Analyses of the North East Atlantic Fauna A peer-reviewed open-access journal ZooKeys 845: 1–97 (2019) Sphaerodoridae in the North East Atlantic 1 doi: 10.3897/zookeys.845.32428 RESEARCH ARTICLE http://zookeys.pensoft.net Launched to accelerate biodiversity research Systematic re-structure and new species of Sphaerodoridae (Annelida) after morphological revision and molecular phylogenetic analyses of the North East Atlantic fauna María Capa1,2, Arne Nygren3, Julio Parapar4, Torkild Bakken2, Karin Meißner5, Juan Moreira6 1 University of the Balearic Islands, Department of Biology, Palma, Spain 2 Norwegian University of Science and Technology, NTNU University Museum, Trondheim, Norway 3 Sjöfartsmuseet Akvariet, Göteborg, Swe- den 4 University of A Coruña, Department of Biology, A Coruña, Spain 5 Forschungsinstitut Senckenberg, Deutsches Zentrum für Marine Biodiversitätsforschung (DZMB), Hamburg, Germany 6 Autonomous Univer- sity of Madrid, Departament of Biology (Zoology), Madrid, Spain Corresponding author: María Capa ([email protected]; [email protected]) Academic editor: Greg Rouse | Received 19 December 2018 | Accepted 25 February 2019 | Published 15 May 2019 http://zoobank.org/F05BDFEC-4C4A-4F22-9685-4AC2655B973D Citation: Capa M, Nygren A, Parapar J, Bakken T, Meißner K, Moreira J (2019) Systematic re-structure and new species of Sphaerodoridae (Annelida) after morphological revision and molecular phylogenetic analyses of the North East Atlantic fauna. ZooKeys 845: 1–97. https://doi.org/10.3897/zookeys.845.32428 Abstract Detailed morphological study of more than 2600 North East Atlantic (NEA) sphaerodorids (Sphaerodori- dae, Annelida) and phylogenetic analyses of DNA sequences of representatives of several identified mor- phospecies enforced changing the current systematic classification within the family, allowed the discovery of new species, provided new information about the morphological and genetic characterisation of mem- bers of this group, and increased the species occurrence data to better infer their geographic and bathym- etric distribution ranges. Phylogenetic analyses of nuclear (18S rRNA and 28S rRNA) and mitochondrial sequences (COI and 16S rRNA) of NEA short-bodied sphaerodorids revealed outstanding results includ- ing paraphyly of the genera Sphaerodoropsis, Sphaerodoridium, and Sphaerephesia. The number of longitu- dinal and transverse rows of dorsal macrotubercles is proposed as potential synapomorphies for the main clades, and are consequently herein used for the genera delimitation. The new classification proposed here implies nomenclatural changes and the erection of a new genus, Geminofilum gen. n., to accommodate the species previously considered as Sphaerodoropsis with two transverse rows of dorsal macrotubercles per Copyright María Capa et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 2 María Capa et al. / ZooKeys 845: 1–97 (2019) segment. Four species are being described herein: Euritmia nordica Capa & Bakken, sp. n., Sphaerephesia multichaeta Capa, Moreira & Parapar, sp. n., Sphaerephesia ponsi Capa, Parapar & Moreira, sp. n., and Sphaerodoridium celiae Moreira, Capa & Parapar, sp. n. Characterisation of the other 21 species, includ- ing updated iconography, and an identification key to all NEA short-bodied sphaerodorids are provided. Keywords 16S rRNA, 18S rRNA, 28S rRNA, classification, COI, identification key, integrative taxonomy, mor- phology, new genus, new species, phylogeny, systematics Table of contents Introduction ............................................................................................................. 2 Materials and methods ............................................................................................. 4 Morphological studies ........................................................................................ 4 DNA sequence analyses ...................................................................................... 5 Results ...................................................................................................................... 7 Phylogenetic analyses ......................................................................................... 7 Atlantic sphaerodorid relationships and subsequent nomenclatural changes ....... 7 Taxonomic accounts ......................................................................................... 10 Identification key to genera and NEA sphaerodorid species .............................. 87 Summary and discussion ........................................................................................ 89 Acknowledgements ................................................................................................. 90 References .............................................................................................................. 91 Introduction Sphaerodoridae Malmgren, 1867 is a relatively small group (approximately 110–120 nominal species) of benthic marine worms, reported worldwide from intertidal to abyssal depths (Capa et al. 2014, 2016a). The monophyly of the group has been as- sessed recently and is evidenced by their well-defined external morphology (Capa et al. 2016a). Sphaerodorids are characterised by the presence of conspicuous epithe- lial tubercles arranged in more or less clear rows (longitudinal and transverse) and a thick cuticle without collagen (e.g., Ruderman 1911, Reimers 1933, Hausen 2005, Filippova et al. 2010, Capa et al. 2014, 2016a). Within Sphaerodoridae, two distinct groups with substantial morphological differences have been distinguished: the long- bodied forms (with elongate and slender bodies, clear segmentation, two longitudinal rows of macrotubercles with terminal papillae and presence of reduced dorsal cirri or microtubercles) and the short-bodied forms (usually measuring less than 5 mm long, with poorly delineated segments and a great variety of number and arrangement of epithelial dorsal tubercles) (Fauchald 1974, Helm and Capa 2015, Capa et al. 2016a). Long-bodied sphaerodorids included members of Ephesiella Chamberlin, 1919, Ephesiopsis Hartman & Fauchald, 1971 and Sphaerodorum Ørsted, 1843, but it has recently been reviewed and all species transferred into the Sphaerodorum (Capa et al. 2018). Monophyly of some short-bodied genera (including Clavodorum Hartman Sphaerodoridae in the North East Atlantic 3 & Fauchald, 1971, Commensodorum Fauchald, 1974, Euritmia Sardá-Borroy, 1987, Sphaerephesia Fauchald, 1972, Sphaerodoridium Lützen, 1961, and Sphaerodoropsis Hartman & Fauchald, 1971) still need assessment (Capa and Bakken 2015, Capa et al. 2016a). The North East Atlantic (NEA), which includes the European part of the Atlantic, is dominated by deep ocean basins, including the Greenland, Lofoten, and Norwegian Basins, with depths down to 5000 m, and a shallow continental shelf along the Eu- ropean coast (Celtic Sea, Bay of Biscay and Iberian coast). This marine region holds a large diversity of Sphaerodoridae (Annelida) compared with other world geographic areas, with 26 species described or reported herein to date (Table 1). This diversity may reflect the collecting effort put into this biogeographic region during the last two centuries and the taxonomic expertise gathered in European countries. Nevertheless, this species list needs revision. Some of the species described and reported from the NEA have a wide distribution range. For instance, Sphaerodoridium minutum (Webster & Benedict, 1887) has been reported in both eastern and western coasts of the North Atlantic and in NEA, from the Arctic to temperate waters and from coastal and shelf habitats (Fauchald 1974). Table 1. Species of Sphaerodoridae (Annelida) (with nomenclature as in Read and Fauchald 2018) re- ported from the North Eastern Atlantic, with type locality and depth. Species Type locality Depth Clavodorum fauchaldi Desbruyères, 1980 Banc Le Danois, Bay of Biscay 1913 m Commensodorum commensalis (Lützen, 1961) Kristineberg, Gullmarfjord, Sweden 35 m Ephesiella abyssorum (Hansen, 1882) Off Møre og Romsdal, Norway 960 m Ephesiella ramosae Desbruyères, 1980 Meriadzek Terrace, Bay of Biscay 2156 m Euritmia hamulisetosa Sardá-Borroy, 1986 Tarifa, Gibraltar Strait 0.5 m Sphaerodoridium claparedii Greeff, 1866 Dieppe, English Channel (?) Sphaerodoridium fauchaldi Hartmann-Schröder, 1993 North Sea 172 m Sphaerodoridium guerritai Moreira & Parapar, 2015 Iceland 600 m Sphaerodoropsis amoureuxi Aguirrezabalaga & Ceberio, 2005 Capbreton Canyon, Bay of Biscay 984–1029 m Sphaerodoropsis artabrensis Moreira & Parapar, 2007 Artabro Gulf, NW Iberian Peninsula 209 m Sphaerodoropsis baltica Reimers, 1933 Kiel, Baltic Sea 6–8 m Sphaerodoropsis chardyi Desbruyères, 1980 Bay of Biscay 2430 m Sphaerodoropsis distichum (Eliason, 1962) Skagerrak 460 m Sphaerodoropsis garciaalvarezi Moreira et al., 2004 Baiona, NW Iberian Peninsula 7 m Sphaerodoropsis gudmunduri Moreira & Parapar, 2012 North Iceland 97 m Sphaerodoropsis halldori Moreira & Parapar, 2012 Western Iceland 1162 m Sphaerodoropsis laureci Desbruyères, 1980 Meriadzek Terrace, Bay of Biscay 2325 m Sphaerodoropsis longipapillata Desbruyères, 1980 Bay of Biscay 4150 m Sphaerodoropsis martinae Desbruyères, 1980 Banc Le Danois, Bay of Biscay 1913 m Sphaerodoridium cf. minutum (Webster & Benedict, 1887) Off New England, USA, continental shelf Sphaerodoropsis philippi (Fauvel, 1911) Kara Sea
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