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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

  • Katrine WorsaaeEmail author
  • Brett C. Gonzalez
  • Alexandra Kerbl
  • Sofie Holdflod Nielsen
  • Julie Terp Jørgensen
  • Maickel Armenteros
  • Thomas M. Iliffe
  • Alejandro Martínez
MeioLanza
Part of the following topical collections:
  1. Interstitial and Cave Diversity in Atlantic Oceanic Islands

Abstract

Anchialine caves have revealed a variety of highly adapted animals including several records of nerillid annelids. However, only one stygobitic lineage, Speleonerilla nom. nov. (previously known as Longipalpa), seems obligate to this environment. We here provide new information on this lineage including the description of three new species, two new records, and the first phylogeny of the genus. All species have been collected from the water column of anchialine caves in the Caribbean, Bermuda, and Canary Islands, contrary to their benthic and interstitial nerillid relatives. New species were described combining light, scanning electron, and confocal laser scanning microscopy and named after traditional dances from their corresponding countries. Speleonerilla isa sp. n. is morphologically the most divergent species, characterized by the presence of nine segments, two pairs of spermioducts, and parapodial cirri present on all segments. Speleonerilla calypso sp. n. and S. salsa sp. n. are mainly distinguished from S. saltatrix by the presence of one additional pair of nephridia and are diagnosed based on unique combinations of characters including the specific arrangements of trunk ciliation, parapodial cirri, and number of chaetae. Two additional records from anchialine caves in Northeast Cuba and México were not described due to limited available material. Phylogenetic analyses of four molecular markers recovered the East Atlantic S. isa as sister to a clade containing the West Atlantic species, the interrelationship of which did not further reflect the geographical distances within the Caribbean. Evolutionary adaptations are discussed, such as the long ciliated palps and pygidial lobes of Speleonerilla used for swimming and their high tolerance to changing salinities when apparently feeding on bacteria in the halocline of the anchialine cave systems.

Keywords

Interstitial Cave fauna Meiofauna Troglomorphism Stygofauna 

Notes

Acknowledgements

We are grateful to Elena Mateo and Leopoldo Moro for the assistance with obtaining the permissions. Special thanks go to the divers Luis E. Cañadas, Enrique Domínguez, Carola D. Jorge, Ralf Schoenemark, and a larger group of international students and colleagues helping us collect and sort out the animals during the First International Workshop to Marine and Anchialine Meiofauna, Lanzarote 2011.

Collection permits for the Bahamas were facilitated by Nancy Albury and Keith Tinker of The National Museum of the Bahamas/The Antiquities, Monuments and Museums Corporation (AMMC), and by the Abaco-based nongovernmental organization Friends of the Environment. A debt of gratitude goes out to Brian Kakuk (Bahamas Underground) as well as the additional cave divers assisting collections, including Lara Hinderstein, Tami Thomsen (Wisconsin Historical Society), and Gregg Stanton (Wakulla Diving Center). Jørgen Olesen (National History Museum Denmark, University of Copenhagen) sorted out and fixed precious samples for CLSM in the field, hereby allowing us to examine the nephridia of S. calypso, for which we are most grateful.

Provision of collection permits in México was facilitated by Fernando Álvarez, Universidad Nacional Autónoma de México to Thomas M. Iliffe (Texas A&M University at Galveston) and collecting was supported financially by grants of the Carlsberg Foundation as well as by the University of Copenhagen.

Collections during two expeditions in Cuba were supported by the Carlsberg Foundation and by an amazing group of divers, colleagues, and students from the Universities of Copenhagen and Havana: Peter Rask Møller, Arturo Regis, Erik García, José Andrés Pérez, Pedro Chevalier, Víctor Isla, Haidi Cecilie Petersen, and Maria Mikkelsen.

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 Cuba and 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. 272060260 to KW) and the Carlsberg Foundation (2010_01_0802 to KW) as well as Consejería de Medio Ambiente del Gobierno de Lanzarote and authorized by Gobierno de Canarias and Centros Turísticos.

Collections in Bahamas received support from the National Science Foundation’s Division of Environmental Biology (NSF DEB-9870219 and DEB-0315903), NOAA’s Caribbean Marine Research Center, and the National Geographic Channel to TMI.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements, if applicable.

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Copyright information

© Senckenberg Gesellschaft für Naturforschung 2018

Authors and Affiliations

  • Katrine Worsaae
    • 1
    Email author
  • Brett C. Gonzalez
    • 1
  • Alexandra Kerbl
    • 1
  • Sofie Holdflod Nielsen
    • 1
  • Julie Terp Jørgensen
    • 1
  • Maickel Armenteros
    • 2
  • Thomas M. Iliffe
    • 3
  • Alejandro Martínez
    • 1
    • 4
  1. 1.Marine Biological Section, Department of BiologyUniversity of CopenhagenCopenhagenDenmark
  2. 2.Centro de Investigaciones MarinasUniversidad de La HabanaHavanaCuba
  3. 3.Department of Marine BiologyTexas A&M University at GalvestonGalvestonUSA
  4. 4.Institute of Ecosystem StudyItalian National Research CouncilVerbaniaItaly

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