Skip to main content
SpringerLink
Log in

Diversity and phylogenetic relationships of North Atlantic Laonice Malmgren, 1867 (Spionidae, Annelida) including the description of a novel species

  • Biodiversity of Icelandic Waters
  • Published:
Marine Biodiversity Aims and scope Submit manuscript

Abstract

Spionid polychaetes are dominant members of many marine soft-bottom communities. As such, understanding their diversity and evolutionary history is of general interest. One spionid group in particular, Laonice, is known from the North Atlantic with several species occurring in deeper waters. We explored, as part of the IceAGE project, the biodiversity and evolution of Laonice using both morphology and mitochondrial cytochrome c oxidase subunit I (COI) gene data. Our data confirm the existence of at least seven lineages of Laonice in waters surrounding Iceland. Additionally, our sampling suggests species distributions of Laonice are similar to previous reports for other annelids, in that warmer waters south of Iceland appear to harbor more species, but further work is needed to clarify distribution patterns. Although our analysis was hampered by quality of preservation of animals from deep water, we recovered several species that were previously known to science (e.g., Laonice blakei, Laonice sarsi, Laonice cf. norgensis, and Laonice cirrata) and one new species. Laonice plumisetosa sp. nov. is characterized by having u-shaped nuchal organs not exceeding chaetiger 1 and the presence of stout capillaries with plush-like texture in parapodia of anterior chaetigers. Uncorrected genetic distances and phylogenetic analyses of COI data confirm these Laonice lineages are distinct. However, L. cirrata is composed of three subclades suggesting unrecognized diversity within this species. In the present paper, we aim to provide a preliminary phylogeny for Laonice and discuss our results in relation to the recently proposed subgenera for Laonice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Blake JA (1994) Family Spionidae. In: Blake JA, Hilbig B, Scott PH (eds) Taxonomic atlas of the Santa Maria Basin and Western Santa Barbara Channel. Volume 6. The Annelida Part 3—Polychaeta: Orbiniidae to Cossuridae. Santa Barbara Museum of Natural History, Santa Barbara, CA, pp 81–224

  • Brasier MJ, Wiklund H, Neal L, Jeffreys R, Linse K, Ruhl H, Glover AG (2016) DNA barcoding uncovers cryptic diversity in 50% of deep-sea Antarctic polychaetes. R Soc Open Sci 3:160432. https://doi.org/10.1098/rsos.160432

    Article  PubMed  PubMed Central  Google Scholar 

  • Brasier MJ, Harle J, Wiklund H, Jeffreys RM, Linse K, Ruhl HA, Glover AG (2017) Distributional Patterns of Polychaetes Across the West Antarctic Based on DNA Barcoding and Particle Tracking Analyses. Front Mar Sci 4:356

  • Brix S, Svavarsson J (2010) Distribution and diversity of desmosomatid and nannoniscid isopods ( Crustacea ) on the Greenland–Iceland–Faroe Ridge. Polar Biol 33:515–530

    Article  Google Scholar 

  • Brix S, Meißner K, Bente S, Halanych KM (2014) The IceAGE project—a follow up of BIOICE. Pol Polar Res 35:141–150

    Article  Google Scholar 

  • Carr CM, Hardy SM, Brown TM, Macdonald TA, Hebert PDN (2011) A tri-oceanic perspective: DNA barcoding reveals geographic structure and cryptic diversity in Canadian Polychaetes. PLoS One. https://doi.org/10.1371/journal.pone.0022232

  • Dahlgren TG, Akesson B, Schander C, Halanych KM, Sundberg P (2001) Molecular phylogeny of the model annelid Ophryotrocha. Biol Bull 201:193–203

    Article  PubMed  CAS  Google Scholar 

  • Delgado-Blas H (2009) Spionidae Grube, 1850. In: de León-González JA, Bastida-Zavala JR, Carrera-Parra LF, García-Garza ME, Peña-Rivera A, Salazar-Vallejo SI, Solís-Weiss V (eds) Poliquetos (Annelida: Polychaeta) de México y América Tropical. Universidad Autónoma de Nuevo León, Monterrey

    Google Scholar 

  • Dijkstra HH, Warén A, Gudmundsson G (2009) Pectinoidea (Mollusca: Bivalvia ) from Iceland. Mar Biol 5:207–243

    Article  Google Scholar 

  • Edgar RC (2004) MUSCLE : multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    PubMed  CAS  Google Scholar 

  • Foster NM (1971) Spionidae (Polychaeta) of the Gulf of Mexico and the Caribbean Sea. Studies on the fauna of Curaçao and other Caribbean Islands. 36:1–183

  • Glover AG, Goetze E, Dahlgren TG, Smith CR (2005) Morphology, reproductive biology and genetic structure of the whale-fall and hydrothermal vent specialist, Bathykurila guaymasensis Pettibone, 1989 (Annelida: Polynoidae). Mar Ecol 26:223–234

    Article  Google Scholar 

  • Greaves E, Meiẞner K, Wilson R (2011) New Laonice species (Polychaeta: Spionidae) from western and northern Australia. Zootaxa 2903:1–20

    Google Scholar 

  • Halanych KM, Janosik AM (2006) A review of molecular markers used for Annelid phylogenetics. Integr Comp Biol 46:533–543

    Article  PubMed  Google Scholar 

  • Hartman O (1965) Deep-water benthic polychaetous annelids off New England to Bermuda and other North Atlantic areas. Occas Pap Allan Hancock Found 1–384

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES : Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Janssen A, Kaiser S, Meißner K, Brenke N, Menot L, Martínez Arbizu P (2015) A reverse taxonomic approach to assess macrofaunal distribution patterns in abyssal pacific polymetallic nodule fields. PLoS One 10:e0117790. https://doi.org/10.1371/journal.pone.0117790

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701

    Article  PubMed  CAS  Google Scholar 

  • Maciolek NJ (2000) New species and records of Aonidella, Laonice, and Spiophanes (Polychaeta: Spionidae) from shelf and slope depths of the Western North Atlantic. Bull Mar Sci 67:529–548

    Google Scholar 

  • Mahon AR, Mahon HK, Dauer DM, Halanych KM (2009) Discrete genetic boundaries of three Streblospio (Spionidae, Annelida) species and the status of S. shrubsolii. Mar Biol Res 5:172–178

    Article  Google Scholar 

  • Malmgren AJ (1867) Annulata Polychaeta Spetsbergiæ, Grœnlandiæ, Islandiæ et Scandinaviæ. Hactenus Cognita. Ex Officina Frenckelliana, Helsingforslæ. 127 pp

  • Meißner K, Blank M (2009) Spiophanes norrisi sp. nov. (Polychaeta: Spionidae) a new species from the NE Pacific coast, separated from the Spiophanes bombyx complex based on both morphological and genetic studies. Zootaxa 2278:1–25

    Google Scholar 

  • Meißner K, Götting M (2015) Spionidae (´Polychaeta´: Canalipalpata) from Lizard Island (Great Barrier Reef, Australia): the genera Malacoceros, Scolelepis, Spio; Microspio, and Spiophanes. Zootaxa 4019(1):378–413

  • Meißner K, Bick A, Guggolz T, Götting M (2014a) Spionidae (Polychaeta: Canalipalpata: Spionida) from seamounts in the NE Atlantic. Zootaxa 3786:201–245

    Article  PubMed  Google Scholar 

  • Meißner K, Brenke N, Svavarsson J (2014b) Benthic habitats around Iceland investigated during the IceAGE expeditions. Polish Polar Res 35:177–202

    Article  Google Scholar 

  • Meißner K, Fiorentino D, Schnurr S, Martinez Arbizu P, Huettmann F, Holst S, Brix S, Svavarsson J (2014c) Distribution of benthic marine invertebrates at northern latitudes—an evaluation applying multi-algorithm species distribution models. J Sea Res 85:241–254

    Article  Google Scholar 

  • Meißner K, Bick A, Götting M (2016) Arctic Pholoe (Polychaeta: Pholoidae): when integrative taxonomy helps to sort out barcodes. Zool J Linnean Soc. https://doi.org/10.1111/zoj.12468

  • Miralles L, Ardura A, Arias A, Borrell YJ, Clusa L, Dopico E, Hernandez de Rojas A, Lopez B, Muñoz-Colmenero M, Roca A, Valiente AG, Zaiko A, Garcia-Vazquez E (2016) Barcodes of marine invertebrates from north Iberian ports : native diversity and resistance to biological invasions. Mar Pollut Bull 112:183–188

    Article  PubMed  CAS  Google Scholar 

  • Ostmann A, Schnurr S, Arbizu PM (2014) Marine environment around Iceland: hydrography, sediments and first predictive models of Icelandic deep-sea sediment characteristics. Polish Polar Res 35:151–176

    Article  Google Scholar 

  • Parapar J (2003) Oweniidae (Annelida, Polychaeta) from Icelandic waters, collected by the BIOICE project, with a description of Myrioglobula islandica n. sp. Sarsia. doi: https://doi.org/10.1080/00364820310002506

  • Parapar J, Moreira J, Helgason GV (2011) Distribution and diversity of the Opheliidae (Annelida, Polychaeta) on the continental shelf and slope of Iceland, with a review of the genus Ophelina in northeast Atlantic waters and description of two new species. Org Divers Evol 11:83–105

    Article  Google Scholar 

  • Radashevsky VI, Lana PC (2009) Laonice (Annelida: Spionidae) from South America. Zoosymposia 2:265–295

    Google Scholar 

  • Radashevsky VI, Neretina TV, Pankova VV, Nuzhdin SV (2014) Molecular identity, morphology and taxonomy of the Rhynchospio glutaea complex with a key to Rhynchospio species (Annelida, Spionidae). Syst Biodivers 12:37–41

    Article  Google Scholar 

  • Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. available from https://tree.bio.ed.ac.uk/software/tracer/

  • Rouse GW (2001) Spionidae. In: Rouse GW, Pleijel F (eds) Polychaetes. Oxford University Press, New York, pp 269–272

    Google Scholar 

  • Sars M (1851) Beretning om en i Sommeren 1849 foretagen zoologisk Reise i Lofoten og Finmarken. Nyt Magazin for Naturvidenskaberne 6:121–211

    Google Scholar 

  • Sigvaldadóttir E (2002) Polychaetes of the genera Prionospio and Aurospio (Spionidae, Polychaeta) from Icelandic waters. Sarsia 87:207–215

    Article  Google Scholar 

  • Sigvaldadóttir E, Desbruyere D (2003) Two new species of Spionidae (Annelida: Polychaeta) from Mid-Atlantic Ridge hydrothermal vents. Cah Biol Mar 44:219–225

    Google Scholar 

  • Sikorski AV (2002) On distinguishing the morphologically close species, Laonice cirrata and L. bahusiensis (Polychaeta, Spionidae). Zoologichesky Zhurnal 81:406–419

    Google Scholar 

  • Sikorski AV (2003a) Laonice (Polychaeta, Spionidae) in the Arctic and the North Atlantic. Sarsia 88:316–345

    Article  Google Scholar 

  • Sikorski AV (2003b) On the fauna of the genus Laonice (Polychaeta, Spionidae) in the northern Pacific. Zoologichesky Zhurnal 82:1179–1190

  • Sikorski AV (2011) Review of Laonice (Spionidae, Annelida) with remarks on several species and a description of a new species from South Africa. Ital J Zool 78:37–41

    Article  Google Scholar 

  • Sikorski AV, Pavlova L (2016) Three new species of Laonice (Polychaete: Spionidae) from West and Southwest Africa. Zootaxa 4097:353–368

    Article  PubMed  Google Scholar 

  • Sikorski AV, Jirkov IA, Tsetlin AB (1988) The genus Laonice (Polychaeta, Spionidae) in the Arctic Ocean: weighing the taxonomic characters and species composition. Zool Zh 67:826–838

    Google Scholar 

  • Sikorski AV, Gunton LM, Pavlova L (2017) Laonice species (Polychaeta, Spionidae) from the Whittard Canyon (NE Atlantic) with descriptions of two new species. J Mar Biol Assoc UK 97:961–973

    Article  CAS  Google Scholar 

  • Söderström A (1920) Studien über die Polychätenfamilie Spionidae. Dissertation Uppsala Almquist & Wicksells:1–286

  • Stransky B, Svavarsson J (2006) Astacilla boreaphilis sp nov. (Crustacea: Isopoda: Valvifera) from shallow and deep North Atlantic waters. Zootaxa 1259:1–23

    Google Scholar 

  • Thornhill DJ, Struck TH, Ebbe B, Lee RW, Mendoza GF, Levin LA, Halanych KM (2012) Adaptive radiation in extremophilic Dorvilleidae (Annelida): diversification of a single colonizer or multiple independent lineages? Ecol Evol 2:1958–1970

    Article  PubMed  PubMed Central  Google Scholar 

  • Wesenberg-Lund E (1950) Polychaeta. Danish Ingolf-Expedition 4:1–92

    Google Scholar 

  • Wilson WH (1991) Sexual reproductive modes in Polychaetes: classification and diversity. Bull Mar Sci 48:500–516

    Google Scholar 

  • Ye L, Cao C, Tang B, Yao T, Wang R, Jiangyong W (2017) Morphological and molecular characterization of Polydora websteri (Annelida: Spionidae), with remarks on relationship of adult worms and larvae using mitochondrial COI gene as a molecular marker. Pak J Zool 49:699–710

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank the technicians of the German Centre of Marine Biodiversity Research (DZMB), Karen Jeskulke, and Antje Fischer for sample management. Dieter Fiege helped with photography and provided the photo of the holotype. Renate Walter (University of Hamburg) kindly assisted with SEM studies. We thank Andrey Sikorski for providing his poster from the IPC2016 meeting as a handout pdf. Saskia Brix and Torben Riehl facilitated visits of V.E.B to Hamburg. We also thank Damien S. Waits and one anonymous reviewer for helpful comments on the manuscript. This work was made possible with the kind support of the crew of the R/V Meteor (M85/3) and R/V Poseidon (POS456). Visits to Hamburg were partially supported by German Research Foundation (DFG) grant BR3843/6–1. This work was funded by National Science Foundation grant DEB-1036537 to K. M. H. and DFG grant BR3843/4–1. This is Molette Biology Laboratory contribution 75 and Auburn University Marine Biology Program contribution 172.

Funding

This study was funded by the National Science Foundation (grant DEB–1036537) and the German Research Foundation (grants: BR3843/4–1, BR3843/6–1).

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Molette Biology Laboratory for Environmental and Climate Change Studies, Auburn University, 101 Rouse Life Sciences Building, Auburn, AL, 36849, USA

    Viktoria E. Bogantes & Kenneth M. Halanych

  2. Forschungsinstitut Senckenberg, Deutsches Zentrum für Marine Biodiversitätsforschung, Biozentrum Grindel, Martin-Luther-King-Platz 3, D-20146, Hamburg, Germany

    Karin Meißner

Authors
  1. Viktoria E. Bogantes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kenneth M. Halanych
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karin Meißner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Viktoria E. Bogantes.

Ethics declarations

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 by the authors.

Sampling and field studies

All necessary permits for sampling have been obtained by the organizers of the cruises (DZMB Hamburg) from the competent authorities.

Additional information

Communicated by S. Brix

This article is part of the Topical Collection on Biodiversity of Icelandic Waters by Karin Meißner, Saskia Brix, Ken M. Halanych, and Anna Jazdzewska.

This article is registered in ZooBank under urn:lsid:zoobank.org:pub:FBEE0FE4-1CDE-4ACD-9FA6-634FCEA690FE

Electronic supplementary material

ESM 1

(DOCX 12 kb)

ESM 2

(XLSX 26 kb)

ESM 3

(GIF 469 kb)

High resolution image (TIFF 124668 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bogantes, V.E., Halanych, K.M. & Meißner, K. Diversity and phylogenetic relationships of North Atlantic Laonice Malmgren, 1867 (Spionidae, Annelida) including the description of a novel species. Mar Biodiv 48, 737–749 (2018). https://doi.org/10.1007/s12526-018-0859-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12526-018-0859-8

Keywords

Search

Navigation