Echinoderes hakaiensis sp. nov.: a new mud dragon (Kinorhyncha, Echinoderidae) from the northeastern Pacific Ocean with the redescription of Echinoderes pennaki Higgins, 1960

  • María Herranz
  • Evgeniya Yangel
  • Brian S. Leander
Original Paper

Abstract

Surveys of kinorhynch diversity in the northeastern Pacific Ocean are rare, and only eight species have been described from the region so far. We explored the diversity of kinorhynchs from a pristine coastal habitat of British Columbia (Calvert Island) and discovered a new subtidal species, Echinoderes hakaiensis sp. nov. We also redescribed one of the oldest described echinoderid species, E. pennaki. Both species were characterized with high-resolution light microscopy (LM), scanning electron microscopy (SEM), and DNA sequences from the mitochondrial cytochrome c oxidase subunit 1 (COI) gene. Echinoderes hakaiensis sp. nov. can be differentiated from other species by a unique pattern of spines and tubes (i.e., four pairs of tubes on segment 2 combined with three middorsal spines). Echinoderes pennaki shows a configuration of traits on segment 2 that questions the reliability of conventional morphological characters used to distinguish different genera within the Echinoderidae. Reevaluation of these characters will require a resolved molecular phylogenetic context including a more comprehensive sampling of species within the group.

Keywords

British Columbia Meiofauna Cyclorhagida COI Systematics 

Notes

Acknowledgments

The authors are grateful to Niels Van Steenkiste for his help during the sampling. Martin V. Sørensen is acknowledged for kindly providing graphic material of different Echinoderes species. We wish to thank the staff at the Bioimaging Facility at the University of British Columbia (UBC) for their help and the staff at Hakai Institute, especially Wayne Jacobs and the Coastal Sand Ecosystems Project members. This work was supported by a grant to BSL from the Tula Foundation (Centre for Microbial Diversity and Evolution), the National Sciences and Engineering Research Council of Canada (NSERC 2014-05258), and the Canadian Institute for Advanced Research, Program in Integrated Microbial Biodiversity.

References

  1. Adrianov AV, Higgins RP (1996) Pycnophyes parasanjuanensis, a new kinorhynch (Kinorhyncha: Homalorhagida: Pycnophyidae) from San Juan Island, Washington, U.S.A. Proc Biol Soc Wash 109(2):236–247Google Scholar
  2. Adrianov AV, Malakhov VV (1994) Kinorhyncha: structure, development, phylogeny and taxonomy. Nauka Publishing, MoscowGoogle Scholar
  3. Adrianov AV, Murakami C, Shirayama Y (2002) Echinoderes aureus n. sp. (Kinorhyncha: Cyclorhagida) from Tanabe Bay (Honshu Island), Japan, with a key to the genus Echinoderes. Spec Div 7(1):47–66Google Scholar
  4. Blake CH (1930) Three new species of worms belonging to the order Echinodera. Biol Survey Mt Desert Region 4:3–10Google Scholar
  5. Brinkhurst RO (1987) Distribution and abundance of macroscopic benthic infauna from the continental shelf off southwestern Vancouver Island, British Columbia. Canadian Technical Report of Hydrography and Ocean Sciences no. 85, 86 ppGoogle Scholar
  6. Claparède ARE (1963) Zur Kenntnis der Gattung Echinoderes Duj. Beobachtungen über Anatomie und Entwicklungsgeschichte wirbelloser Thiere: an der Küste von Normandie angestellt. Verlag von Wilhelm Engelmann, Leipzig, pp 90–92, 119, pls XVI–XVIIGoogle Scholar
  7. Folmer O, Black M, Hoeh W et al (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  8. Greeff R (1869) Untersuchungen über einige merkwürdige Thiergruppen des Arthropoden- und Wurm-Typus. Arch Naturgesch 35:71–121Google Scholar
  9. Grzelak K, Sørensen MV (2017) New species of Echinoderes (Kinorhyncha: Cyclorhagida) from Spitsbergen, with additional information about known Arctic species. Mar Biodiv (in press)Google Scholar
  10. Herranz M, Leander BS (2016) Redescription of Echinoderes ohtsukai Yamasaki and Kajihara, 2012 and E. kozloffi Higgins, 1977 from the northeastern Pacific coast, including the first report of a potential invasive species of kinorhynch. Zool Anz 265:108–126CrossRefGoogle Scholar
  11. Herranz M, Thormar J, Benito J et al (2012) Meristoderes gen. nov., a new kinorhynch genus, with the description of two new species and their implications for echinoderid phylogeny (Kinorhyncha: Cyclorhagida, Echinoderidae). Zool Anz 251:161–179CrossRefGoogle Scholar
  12. Higgins RP (1960) A new species of Echinoderes (Kinorhyncha) from Puget Sound. Trans Am Microsc Soc 79:85–91CrossRefGoogle Scholar
  13. Higgins RP (1961) Three new homalorhage kinorhynchs from the San Juan Archipelago, Washington. J Elisha Mitchell Sci Soc 77:81–88Google Scholar
  14. Higgins RP (1964a) A method for meiobenthic invertebrate collection. Amer Zool 4(3):291Google Scholar
  15. Higgins RP (1964b) Redescription of the kinorhynch Echinoderes remanei (Blake, 1930) Karling, 1954. Trans Am Microsc Soc 83(2):243–247CrossRefGoogle Scholar
  16. Higgins RP (1967) The Kinorhyncha of New-Caledonia. In: Expédition Française sur les Recifs coralliens de la Nouvelle-Calédonie 2. Fondation Singer-Polignac, Paris, pp. 75–90Google Scholar
  17. Higgins RP (1977) Redescription of Echinoderes dujardinii (Kinorhyncha) with descriptions of closely related species. Smithson Contrib Zool 248:1–26CrossRefGoogle Scholar
  18. Higgins RP (1978) Echinoderes gerardi n. sp. and E. riedli (Kinorhyncha) from the Gulf of Tunis. Trans Am Microsc Soc 97(2):171–180CrossRefGoogle Scholar
  19. Higgins RP (1983) The Atlantic Barrier Reef ecosystem at Carrie Bow Cay, Belize, II: Kinorhyncha. Smithson Contrib Mar Sci 18:1–131CrossRefGoogle Scholar
  20. Higgins RP (1986) A new species of Echinoderes (Kinorhyncha: Cyclorhagida) from a coarse-sand California beach. Trans Am Microsc Soc 105(3):266–273CrossRefGoogle Scholar
  21. Higgins RP, Korczynski RE (1989) Two new species of Pycnophyes (Homalorhagida, Kinorhyncha) from the Canadian coast of the Beaufort Sea. Can J Zool 67:2056–2064CrossRefGoogle Scholar
  22. Higgins RP, Kristensen RM (1988) Kinorhyncha from Disko Island, West Greenland. Smithson Contrib Zool 458:1–56CrossRefGoogle Scholar
  23. Huys R, Coomans A (1989) Echinoderes higginsi sp. n. (Kinorhyncha, Cyclorhagida) from the southern North Sea with a key to the genus Echinoderes Claparède. Zool Scr 18(2):211–221CrossRefGoogle Scholar
  24. Jørgensen M, Kristensen RM (1991) Meiofauna investigations from Igloolik, N.W.T. Arctic Canada. In: Jørgensen M (ed) Arctic biology course 1989, Igloolik, N.W.T., Canada. University of Copenhagen Zoological Museum, pp 61–80Google Scholar
  25. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649CrossRefPubMedPubMedCentralGoogle Scholar
  26. Landers SC, Sørensen MV (2016) Two new species of Echinoderes (Kinorhyncha, Cyclorhagida), E. romanoi sp. n. and E. joyceae sp. n., from the Gulf of Mexico. ZooKeys 594:51–71CrossRefGoogle Scholar
  27. Neuhaus B (2013) Kinorhyncha (=Echinodera). In: Schmidt-Rhaesa A (ed) Handbook of zoology: Gastrotricha, Cycloneuralia and Gnatifera. Volume 1: Nematomorpha, Priapulida, Kinorhyncha, Loricifera. Walter de Gruyter, Berlin, pp 1–168Google Scholar
  28. Neuhaus B, Blasche T (2006) Fissuroderes, a new genus of Kinorhyncha (Cyclorhagida) from the deep sea and continental shelf of New Zealand and from the continental shelf of Costa Rica. Zool Anz 245:19–52CrossRefGoogle Scholar
  29. Ostmann A, Nordhaus I, Sørensen MV (2012) First recording of kinorhynchs from java, with the description of a new brackish water species from a mangrove-fringed lagoon. Mar Biodivers 42:79–91CrossRefGoogle Scholar
  30. Pardos F, Higgins RP, Benito J (1998) Two new Echinoderes (Kinorhyncha, Cyclorhagida) from Spain, including a reevaluation of Kinorhynch taxonomic characters. Zool Anz 237:195–208Google Scholar
  31. Pardos F, Sánchez N, Herranz M (2016a) Two sides of a coin: the phylum Kinorhyncha in Panama. I) Caribbean Panama. Zool Anz 265:3–25CrossRefGoogle Scholar
  32. Pardos F, Herranz M, Sánchez N (2016b) Two sides of a coin: the phylum Kinorhyncha in Panama. II) Pacific Panama. Zool Anz 265:26–47CrossRefGoogle Scholar
  33. Sørensen MV (2006) New Kinorhynchs from Panama, with a discussion of some phylogenetically significant cuticular structures. Meiofauna Mar 15:51–77Google Scholar
  34. Sørensen MV, Dal Zotto M, Rho HS et al (2015) Phylogeny of Kinorhyncha based on morphology and two molecular loci. PLoS One 10:e0133440CrossRefPubMedPubMedCentralGoogle Scholar
  35. Sørensen MV, Herranz M, Landers SC (2016) A new species of Echinoderes (Kinorhyncha: Cyclorhagida) from the Gulf of Mexico, with a redescription of Echinoderes bookhouti Higgins, 1964. Zool Anz 265:48–68CrossRefGoogle Scholar
  36. Sørensen MV, Pardos F (2008) Kinorhynch systematics and biology—an introduction to the study of kinorhynchs, inclusive identification keys to the genera. Meiofauna Mar 16:21–73Google Scholar
  37. Sørensen MV, Rho HS, Min WG, Kim D, Chang CY (2012) An exploration of Echinoderes (Kinorhyncha: Cyclorhagida) in Korean and neighboring waters, with the description of four new species and a redescription of E. tchefouensis Lou, 1934. Zootaxa 3368:161–196Google Scholar
  38. Yamasaki H, Kajihara H (2012) A new brackish-water species of Echinoderes (Kinorhyncha: Cyclorhagida) from the Seto Inland Sea, Japan. Spec Div 17:109–118CrossRefGoogle Scholar
  39. Yamasaki H, Hiruta SF, Kajihara H (2013) Molecular phylogeny of kinorhynchs. Mol Phylogenet Evo 67:303–310CrossRefGoogle Scholar
  40. Zelinka C (1894) Über die Organisation von Echinoderes. Ver Dtsch Zool Ges 4:46–49Google Scholar
  41. Zelinka C (1896) Demonstration der Tafeln der Echinoderes—Monographie. Ver Dtsch Zool Ges 6:197–199Google Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • María Herranz
    • 1
  • Evgeniya Yangel
    • 1
  • Brian S. Leander
    • 1
  1. 1.Departments of Zoology and BotanyUniversity of British ColumbiaVancouverCanada

Personalised recommendations