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Description of six new species of Mesonerilla (Nerillidae, Annelida) and an emended description of M. intermedia Wilke, 1953, from marine and cave environments

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Abstract

Nerillidae is a species-rich family of meiofaunal, mainly interstitial annelids. The genus Mesonerilla previously contained eight described species. We here describe six new species of Mesonerilla based on detailed morphological light and scanning electron microscopy studies. The new species were collected from coastal subtidal and tidal sediments, as well as from anchialine caves, in the Mediterranean, Canary Islands, Panamá, Trinidad and Tobago and the USA. All species of Mesonerilla contain nine segments, two-three antennae, two club-shaped palps, parapodial cirri and compound chaetae in most segments. New species are diagnosed by unique character traits and/or a unique combination of characters involving differences in shape of appendages, reproductive characters and glandular and ciliary patterns. Their validation is further supported by a molecular phylogeny including these and the majority of described species of Mesonerilla. With most of the diagnostic characters of the described species being hardly discernible, and with potential additional molecular identifiable species left undescribed, the genus Mesonerilla, as many other interstitial groups, show a high degree of cryptic diversity.

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References

  • Bailey-Brock JH (1999) Nerillidae of Hawai’i: two new records of interstitial polychaetes. Pac Sci 53:299–304

    Google Scholar 

  • Besteiro C, Núñez J, Martínez A (2012) Familia Nerillidae Levinsen, 1883 In Annelida Polychaeta III. Parapar J, Alós C, Núñez J, Moreira J, López E, Aguirrezabalaga F, Besteiro C, Martínez. A. fauna Ibérica vol. 36. MA Ramos et al. (Eds.). Museo Nacional de Ciencias Naturales. CSIC. Madrid:335–345

  • Curini-Galletti M, Artois T, Delogu V, De Smet WH, Fontaneto D, Jondelius U, Leasi F, Martínez A, Meyer-Wachsmuth I, Nilsson KS, Tongiorgi P, Worsaae K, Todaro MA (2012) Patterns of diversity in soft-bodied meiofauna: dispersal ability and body size matter. PLoS One 7(3):e33801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Domenico M, Martínez A, Lana PC, Worsaae K (2014) Molecular and morphological phylogeny of Saccocirridae (Annelida) reveals two cosmopolitan clades with specific habitat preferences. Mol Phylogenet Evol 75:202–218

    Article  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39(4):783–791

    Article  PubMed  Google Scholar 

  • Fenchel T, Finlay BJ (2004) The ubiquity of small species: patterns of local and global diversity. BioScience 54:777

    Article  Google Scholar 

  • Fontaneto D (2011) Biogeography of microscopic organisms: is everything small everywhere? Cambridge University Press

  • Fransen ME (1980) Ultrastructure of coelomic organization in annelids. Zoomorphologie 95:235–249

    Article  Google Scholar 

  • Fransen ME (1983) Fine structure of the brooding apparatus of the Archiannelid Mesonerilla intermedia: maternal connections to brooded eggs. Trans Am Microsc Soc 102:25–37

    Article  Google Scholar 

  • García-Valdecasas A (1985) Estudio faunístico de la cueva submarina "Túnel de la Atlántida", Jameos del Agua, Lanzarote. Nat Hisp 27:1–56

    Google Scholar 

  • Gobert S, Reygel P, Artois T (2019) Schizorhynchia (Platyhelminthes Rhabdocoela) of Lanzarote (Canary Islands), with the description of eight new species. Mar Biodivers 49(5) https://doi.org/10.1007/s12526-017-0736-x

  • Higgins RP, Thiel H (1988) Introduction to the study of Meiofauna. Smithsonian Institution Press, Washington, DC 488 pages

    Google Scholar 

  • Jörger KM, Norenburg JL, Wilson NG, Schrödl M (2012) Barcoding against a paradox? Combined molecular species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugs. BMC Evol Biol 12:245

    Article  PubMed  PubMed Central  Google Scholar 

  • Jouin C (1963) Mesonerilla biantennata n. sp. nouvelle Archiannélide Nerillidae de la region de Roscoff. CR Acad Sci (Paris) D 257:4057–4060

    Google Scholar 

  • Jouin C (1968) Sexualité et biologie de la reproduction chez Mesonerilla Remane et Meganerilla Boaden (Archiannélides, Nerillidae). Cah Biol Mar 6:31–52

    Google Scholar 

  • Jouin C (1970) Archiannélides interstitielles de Nouvelle- Calédonie. Editions de la Fondation Singer-Polignac 4:149–167

    Google Scholar 

  • Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9(4):286–298

    Article  CAS  PubMed  Google Scholar 

  • Katoh K, Kuma KI, TohH MT (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33(2):511–518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katoh K, Asimenos G, Toh H (2010) Multiple alignment of DNA sequences with MAFFT. In: Posada D (ed) Bioinformatics for DNA sequence analysis. Methods in molecular biology (methods and protocols) 537. Humana, New York, pp 39–64

    Google Scholar 

  • Kerbl A, Bekkouche N, Worsaae K (2015) Detailed reconstruction of the nervous and muscular system of Lobatocerebridae with an evaluation of its annelid affinity. BMC Evol Biol 15:277

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lévi C (1953) Archiannélides Nerillidae de la region de Roscoff. Arch Zool Exp Gén 90:64–70

    Google Scholar 

  • Levinsen GMR (1883) Systematisk-geografisk oversigt over de nordiske Annulata, Gephyrea, Chaetognathi og Balanoglossi. Første Halvdel. Vid Medd Dansk Naturh For

  • Martínez A, Palmero AM, Brito MC, Núñez J, Worsaae K (2009) Anchialine fauna of the Corona lava tube (Lanzarote, Canary Islands): diversity, endemism and distribution. Mar Biodivers 39:169–187

    Article  Google Scholar 

  • Martínez A, Di Domenico M, Leasi F, Curini-Galletti M, Todaro MA, Dal Zotto M, Artois T, Norenburg J, Jörger KM, Núñez J, Fontaneto D, Worsaae K (2019) Patterns of diversity and endemismof soft-bodied meiofauna in an oceanic island, Lanzarote, Canary Islands. Mar Biodivers 49(5). https://doi.org/10.1007/s12526-019-01007-0

  • Martínez A, Di Domenico M, Jörger K, Norenburg J, Worsaae K (2013) Description of three new species of Protodrilus (Annelida, Protodrilidae) from Central America. Mar Biol Res 9(7):676–691

    Article  Google Scholar 

  • Martínez A, Di Domenico M, Rouse GW, Worsaae K (2015) Phylogeny of Protodrilidae (Annelida) inferred by total evidence analyses. Cladistics 31:250–276

    Article  PubMed  Google Scholar 

  • Martínez A, Gonzalez BC, Núñez J, Wilkens H, Oromí P, Iliffe TM, Worsaae K (2016) Guide to the anchialine ecosystems of Los Jameos del Agua and Túnel de la Atlántida. Medio Ambiente, Cabildo de Lanzarote, Arrecife, Lanzarote, Spain, 310 pages, ISBN-13: 978-84-95938-92-3

  • Martínez A, Kvindebjerg K, Iliffe TM, Worsaae K (2017) Evolution of cave suspension feeding in Protodrilidae (Annelida). Zool Scr 46(2):214–226

    Article  Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop (GCE)

  • Mills S, Alcántara-Rodríguez JA, Ciros-Pérez J et al (2017) Fifteen species in one: deciphering the Brachionus plicatilis species complex (Rotifera, Monogononta) through DNA taxonomy. Hydrobiologia 796:39–58

    Article  CAS  Google Scholar 

  • Müller MCM (1999) Das Nervensystem der Polychaeten: Immunohistochemische Untersuchungen an ausgewählten Taxa. PhD thesis, University of Osnabrück: 402 pages

  • Núñez J, Ocaña Ó, Brito MC (1997) Two new species (Polychaeta: Fauveliopsidae and Nerillidae) and other polychaetes from the marine lagoon cave of Jameos del Agua, Lanzarote (Canary Islands). Bull Mar Sci 60(2):252–260

    Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25(7):1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53(5):793–808

    Article  PubMed  Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer v1. 4: MCMC trace analyses tool. In http://tree.bio.ed.ac.uk/software/tracer. Accessed 19 Dec 2016

  • Remane A (1949) Archianneliden der Familie Nerillidae aus Südwest-Afrika. Kiel Meeresfors 6:45–50

    Google Scholar 

  • Riser NW (1988) Morphology of a new species of Nerillid Polychaete from the north shore of Massachusetts Bay, U.S.A. Trans Am Microsc Soc 107:171–179

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22(21):2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Struck TH, Feder JL, Bendiksby M, Birkeland S, Cerca J, Gusarov VI, Kistenich S, Larsson KH, Liow LH, Nowak MD, Stedje B, Bachmann L, Dimitrov D (2018) Finding evolutionary processes hidden in cryptic species. Trends Ecol Evol 33(3):153–163

    Article  PubMed  Google Scholar 

  • Swedmark B (1959) Archiannélides Nerillidae des côtes du Finistère. Arch Zool Exp Gén 98:26–42

    Google Scholar 

  • Westheide W (2008) Polychaetes: Interstitial Families. Synopsis of the British Fauna (New Series), 44 (second edition). Field Studies Council: Shrewsbury, UK. ISBN 978–1–85153-271-1. VII, 169 pp

  • Westheide W, Riser NW (1983) Morphology and phylogenetic relationships of the neotenic interstitial polychaete Apodotrocha progenerans n. gen., n. sp. (Annelida). Zoomorphology 103:67–87

    Article  Google Scholar 

  • Wilke U (1953) Mesonerilla intermedia nov. sp., ein neuer Archiannelide aus dem Golf von Neapel. Zool Anz 150:211–215

  • Wilkens H, Iliffe TM, Oromí P, Martínez A, Tysall TN, Koenemann S (2009) The Corona lava tube, Lanzarote: geology, habitat diversity and biogeography. Mar Biodivers 39(3):155–167

    Article  Google Scholar 

  • Worsaae K (2005a) Systematics of Nerillidae (Polychaeta, Annelida). Meiofauna Mar 14:49–74

    Google Scholar 

  • Worsaae K (2005b) Phylogeny of Nerillidae (Polychaeta, Annelida) as inferred from combined 18S rDNA and morphological data. Cladistics 21:143–162

    Article  PubMed  Google Scholar 

  • Worsaae K (2014) Nerillidae Levinsen, 1883. In: Beutel RG, Kristensen NP, Leschen R, Purschke W, Westheide W, Zachos F (eds) Handbook of Zoology online. Walter de Gruyter, Berlin

    Google Scholar 

  • Worsaae K, Kristensen RM (2005) Evolution of interstitial Polychaeta (Annelida). Hydrobiol 535:319–340

    Google Scholar 

  • Worsaae K, Müller MCM (2004) Nephridial and gonoduct distribution patterns in Nerillidae (Annelida: Polychaeta) examined by tubulin staining and cLSM. J Morph 261:259–269

    Article  PubMed  Google Scholar 

  • Worsaae K, Rouse GW (2009) Mesonerilla neridae sp. nov. (Nerillidae): first meiofaunal annelid from deep-sea hydrothermal vents. Zoosymposia 2:297–303

    Article  Google Scholar 

  • Worsaae K, Martínez A, Núñez J (2009) Nerillidae (Annelida) from the Corona lava tube, Lanzarote with description of Meganerilla cesari n. sp. Mar Biodivers 39:195–207

    Article  Google Scholar 

  • Worsaae K, Gonzalez BC, Kerbl A, Nielsen SH, Jørgensen JT, Armenteros M, Iliffe TM, Martínez A (2019). Diversity and evolution of the stygobitic Speleonerilla nom. nov. (Nerillidae, Annelida) with description of three new species from anchialine caves in the Caribbean and Lanzarote. Mar Biodivers 49(5) https://doi.org/10.1007/s12526-018-0906-5

  • Worsaae K, Giribet G, Martínez A (2018) The role of progenesis in the diversification of the interstitial annelid lineage Psammodrilidae. Invert Syst 32:774–793

    Article  Google Scholar 

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Acknowledgements

First of all, we would like to thank Christopher Laumer for collecting and photographing the specimens of the new species M. laerkae and Greg Rouse for collecting some of the examined material of M. intermedia. We greatly acknowledge the many colleagues and students who have helped over more than 10 years of specimen collection for this study, during trips arranged by KW and AM. We are grateful to Elena Mateo and Leopoldo Moro for assistance with obtaining the permissions to sample in Lanzarote, as well as to divers Luis E. Cañadas, Enrique Domínguez, Carola D. Jorge, Ralf Schoenemark and a larger group of international students and colleagues in helping us collect and sort out the animals during the First International Workshop to Marine and Anchialine Meiofauna, Lanzarote 2011. The workshop was funded by Consejería de Medio Ambiente del Cabildo de Lanzarote and Reserva de la Biosfera. We thank Thomas M Iliffe, Terence Tysall, Tim Rozzi and Jill Heinerth for collecting samples from Montaña de Arena in 2008, as well as to Jorge Núñez Fraga for the donation of his material from Los Jameos del Agua. Finally, we are also grateful for the invitation to participate in trips organised by our colleagues Jon Norenburg (to STRI, Panamá), Greg Rouse (to the Great Barrier Reef, Australia), Marco Curini-Galletti (to Sardinia, Italy) and Maikon Di Domenico (to Napoli, Italy).

Funding

Funding of the more than seven expeditions over 8 years was made possible through numerous agencies with the most recent laboratory and expedition costs to México being covered by the Carlsberg Foundation (grants: 2013_01_0779 to AM and CF_0946 and 2013_01_0501 to KW) as well as supported through salaries and administration of the University of Copenhagen to KW, BCG and colleagues. Collections in Lanzarote and secondary laboratory costs were financially supported by the Danish Research Council (grant no. 272–06–0260 to KW) and the Carlsberg Foundation (2010_01_0802 to KW) as well as Consejería de Medio Ambiente del Gobierno de Lanzarote and authorised by Gobierno de Canarias and Centros Turísticos. AM was supported by Marie Skolodowska-Curie Individual Grant (IF-EF), H2020 Program of the EU, number 745530—“ANCAVE—Anchialine caves to understand evolutionary processes”.

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Authors and Affiliations

  1. Marine Biological Section, Department of Biology, University of Copenhagen, Universitetsparken 4, DK-2100, Copenhagen, Denmark

    Katrine Worsaae, Maria Damsgaard Mikkelsen & Alejandro Martínez

  2. Institute for Water Research, National Research Council of Italy, Largo Tonolli 50., 28922, Verbania, Italy

    Alejandro Martínez

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  1. Katrine Worsaae
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  2. Maria Damsgaard Mikkelsen
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Correspondence to Katrine Worsaae.

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Worsaae, K., Mikkelsen, M.D. & Martínez, A. Description of six new species of Mesonerilla (Nerillidae, Annelida) and an emended description of M. intermedia Wilke, 1953, from marine and cave environments. Mar Biodiv 49, 2141–2165 (2019). https://doi.org/10.1007/s12526-019-00984-6

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