Marine Biodiversity

, Volume 48, Issue 1, pp 217–230 | Cite as

Phylogenetic relationships within the Cyatholaimidae (Nematoda: Chromadorida), the taxonomic significance of cuticle pore and pore-like structures, and a description of two new species

  • Daniel Leduc
  • Zeng Qi Zhao
Original Paper


The family Cyatholaimidae Filipjev, 1918 is a relatively diverse group of mainly marine nematodes which has been shown to be monophyletic by morphological and molecular phylogenetic analyses. There are, however, no morphological synapomorphies for any of the four subfamilies that currently comprise the Cyatholaimidae. The two types of cuticle pore and pore-like structures often observed in cyatholaimids may be of taxonomic significance, but the terminology used is inconsistent, and their description is often too limited to provide sufficient information for comparisons. Here, we describe two new cyatholaimid species, Paracanthonchus miltommatus sp. n. and Metacyatholaimus delicatus sp. n., from intertidal and upper continental slope sediments of New Zealand, and investigate the distribution and morphology of cuticle pore and pore-like structures in these two new species using light and scanning electron microscopy. We also investigate phylogenetic relationships within the Cyatholaimidae using SSU and D2-D3 of LSU rDNA sequences. The first type of cuticle structure, first termed pore complex by Wright & Hope (Can J Zool 46:1005–1011, 1968), consists of circular structures usually arranged in sublateral, subventral and subdorsal longitudinal rows, with a slit-like pore and ring-like development of dense material in the middle cuticle layer and typically associated with an underlying cell. The second, less studied type, for which we propose the term lateral pore-like structure, consists of structures arranged along the mediolateral lines in one or more longitudinal rows or sometimes irregularly, usually with a central, non-cuticularised dome, and a round or elliptical cuticularised opening supported by unmodified or modified punctations at anterior and posterior extremities. The function of the lateral pore-like structures remains unclear but their morphology is inconsistent with their descriptions as pores or modified punctations by some authors. The limited information available suggests that the number, distribution, and morphology of pore complexes and lateral pore-like structures could provide taxonomically useful information for defining cyatholaimid genera such as Longicyatholaimus Micoletzky, 1924 and Marylynnia (Hopper, 1972). Our SSU-based molecular phylogenetic analysis retrieved two monophyletic clades with low support, which approximately correspond to the subfamilies Paracanthonchinae and Cyatholaiminae; however, we found that Praeacanthonchus, which is currently classified with the Cyatholaiminae based on the structure of the gubernaculum, may be better placed in the subfamily Paracanthonchinae. This finding suggests that the gubernaculum structure may not be a meaningful character for defining cyatholaimid subfamilies or genera. Features of the cuticle, some of which are already used for defining genera such as Metacyatholaimus Schuurmans Stekhoven, 1942, may better represent phylogenetic relationships within the family, and should, therefore, be described more comprehensively in the future.


Small subunit (SSU) 18S rDNA gene D2-D3 region of large subunit (LSU) 28S rDNA gene Scanning electron microscopy Paracanthonchus miltommatus sp. n Metacyatholaimus delicatus sp. n Pore complexes Lateral pore-like structures Campaniform-type organs 



This research was funded by the NIWA under Coasts and Oceans research programmes Marine Biological Resources and Ocean Flows and Productivity, and was supported by core funding for Crown Research Institutes from the Ministry of Business, Innovation and Employment’s Science and Innovation Group. We thank the scientific personnel, officers and crew of RV Tangaroa of NIWA voyage TAN1506, and in particular Scott Nodder (NIWA) for obtaining the core samples. We are also grateful to Janet Grieve (NIWA) for fruitful discussions. We are grateful to three anonymous reviewers for their constructive criticisms of the manuscript.


  1. Chitwood BG (1933) A revised classification of the Nematoda. J Parasitol 20:131Google Scholar
  2. Chitwood BG, Chitwood MB (1950) Introduction to nematology. University Park Press, BaltimoreGoogle Scholar
  3. Coomans A (1979) A proposal for a more precise terminology of the body regions in the nematode. Annales de la Société Royale Zoologique de Belgique 108:115–117Google Scholar
  4. De Coninck LA (1965) Classe des Nématodes: Systématique des Nématodes et sous-classe des Adenophorea. Traité de Zoologie, GRASSE 4(2):586–681Google Scholar
  5. Decraemer W, Smol N (2006) Orders Chromadorida, Desmodorida and Desmoscolecida. In: Eyualem Abebe A, Tranpurger W, Andràssy I (eds) Freshwater nematodes: Ecology and taxonomy. CABI, Wallingford, pp 497–573CrossRefGoogle Scholar
  6. Filipjev IN (1918) Free-living marine nematodes of the Sevastopol area. Trans Zool Lab Sevastopol Biol Stat Rus Acad Sci 2(4):1–255Google Scholar
  7. Gourbault N (1980) Nématodes abyssaux (Campagne Walda du navire oceanographique Jean-Charcot). I. Espèces nouvelles de Cyatholaimidae. Cah Biol Mar 21:61–71Google Scholar
  8. Holterman M, Van Der Wurff A, Van Den Elsen S, Van Megen H, Bongers T, Holovachov O, Bakker J, Helder J (2006) Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Mol Biol Evol 13:1792–1800CrossRefGoogle Scholar
  9. Holterman M, Holovachov O, van den Elsen S, van Megen H, Bongers T, Bakker J, Helder J (2008) Small subunit ribosomal DNA-based phylogeny of basal Chromadoria (Nematoda) suggests that transitions from marine to terrestrial habitats (and vice-versa) require relatively simple adaptations. Mol Phylogenet Evol 48:758–763CrossRefPubMedGoogle Scholar
  10. Hopper BE (1972) Free-living nematodes from Biscayne Bay, Florida. IV. Cyatholaimidae: on the occurrence of Marilynia n. gen. and Longicyatholaimus Micoletzky, 1924 in Biscayne Bay, with a description of L. longicaudatus (de Man, 1876) from the type locality. Zool Anz 189:64–88Google Scholar
  11. Inglis WG (1963) ‘Campaniform-type’ organs in nematodes. Nature 197:618CrossRefGoogle Scholar
  12. Inglis WG (1970) Cyatholaimidae (Nematoda) from the coast of western Australia. Rec South Aust Museum 16:1–13Google Scholar
  13. Kito K (1981) Studies on the free-living marine nematodes from Hokkaido, IV. J Facult Sce, Hokkaido Univ Ser VI, Zool 22:250–278Google Scholar
  14. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace LM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948CrossRefPubMedGoogle Scholar
  15. Lorenzen S (1981) Entwurf eines phylogenetischen systems der freilebenden nematoden. Veröffentlichungen de Instituts für Meeresforschung in Bremerhaven 7:Suppl. 472SGoogle Scholar
  16. Mawson PM (1953) Some marine freeliving nematodes from the Australia coast. Trans R Soc South Aust 76:34–40Google Scholar
  17. Mayr E (1969) Principles of Systematic Zoology. McGraw-Hill, New YorkGoogle Scholar
  18. Meldal BHM, Debenham NJ, De Ley P, De Ley IT, Vanfleteren JR, Vierstraete AR, Bert W, Borgonie G, Moens T, Tyler PA, Austen MC, Blaxter ML, Rogers AD, Lambshead PJD (2007) An improved molecular phylogeny of the Nematoda with special emphasis on marine taxa. Mol Phylogenet Evol 42:622–636CrossRefPubMedGoogle Scholar
  19. Micoletzky H (1924) Letzter Bericht über freilebende Nematoden aus Suez. Sitzungsberichte der Akademie der Wissenschaften in Wien. Math-Naturwissenschaftliche Klasse 1(133):137–179Google Scholar
  20. Miljutina MA, Miljutin DM (2015) A revision of the genus Paracanthonchus (Cyatholaimidae, Nematoda) with a tabular key to species and a description of P. mamubiae sp. n. from the deep North-Western Pacific. Deep-Sea Res II 111:104–118CrossRefGoogle Scholar
  21. Nunn GB (1992) Nematode molecular evolution. Dissertation, University of NottinghamGoogle Scholar
  22. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  23. Rambaut A, Drummond AJ (2007) Tracer v 1.4, Available from
  24. Ronquist F, Huelsenbeck JP (2003) MR BAYES: Bayesian inference of phylogenetic trees. Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
  25. Schuurmans Stekhoven JH (1942) The free living nematodes of the Mediterranean. III. The Balearic Islands. Zoöl Mededeelingen 23(3–4):229–262Google Scholar
  26. Schuurmans Stekhoven JH (1950) The freeliving marine nemas of the Mediterranean I. The Bay of Villefranche. Mémoires de l’Institut Royal Des Sciences Naturelles de Belgique 2(37):1–220Google Scholar
  27. Sharma J, Hopper BE, Webster JM (1979) Benthic nematodes from the Pacific coast with special reference to the cyatholaimids. Annales de la Société Royale Zoologique de Belgique 108:47–56Google Scholar
  28. Somerfield PJ, Warwick RM (1996) Meiofauna in Marine Pollution Monitoring Programmes: a Laboratory Manual. Ministry of Agriculture, Fisheries and Food, LowestoftGoogle Scholar
  29. Swofford DL (2002) (PAUP*) Phylogenetic Analysis Using Parsimony (and Other Methods), Version 4. Sinauer Associates, SunderlandGoogle Scholar
  30. Tchesunov AV (2014) Order Chromadorida Chitwood, 1933. In: Schmidt-Rhaesa A, (ed) Handbook of Zoology, Gastrotricha, Cyclioneuralia and Gnathifera. Volume 2: Nematoda. CABI Publishing, Cambridge, 373–398Google Scholar
  31. Van Megen H, van den Elsen S, Holterman M, Karssen G, Mooyman P, Bongers T, Holovachov O, Bakker J, Helder J (2009) A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11:927–950CrossRefGoogle Scholar
  32. Vidaković J, Traviz A, Boucher G (2003) Two new species of the genus Metacyatholaimus (Nematoda, Cyatholaimidae) from the Adriatic Sea with a key to the species. Cah Biol Mar 44:111–120Google Scholar
  33. Vincx M, Sharma J, Smol N (1982) On the identity and nomenclature of Paracanthonchus caecus (Bastian, 1865), with a redefinition of the genus Paracanthonchus Micoletzky (Nematoda, Cyatholaimidae). Zool Scr 11:243–263CrossRefGoogle Scholar
  34. Warwick RM (1971) The Cyatholaimidae (Nematoda, Chromadoroidea) off the coast of Northumberland. Cah Biol Mar 12:95–110Google Scholar
  35. Wieser W (1954) Reports of the Lund University Expedition 1948–49 17. Free-living nematodes II. Chromadoroidea. Lunds Universitets Arsskrift N F 50:1–148Google Scholar
  36. Wieser W (1959) Free-living nematodes and other small invertebrates of Puget Sound beaches. Univ Washington Publ Biol 19:1–179Google Scholar
  37. Wright KA, Hope WD (1968) Elaboration of the cuticle of Acanthonchus duplicatus Wieser, 1959 (Nematoda: Cyatholaimidae) as revealed by light and electron microscopy. Can J Zool 46:1005–1011CrossRefGoogle Scholar
  38. Zheng JW, Subbotin SA, He SS, Gu JF, Moens M (2002) Molecular characterisation of some Asian isolates of Bursaphelenchus xylophilus and B. mucronatus using PCR-RFLPs and sequences of ribosomal DNA. Russ J Nematol 11:17–22Google Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.National Institute of Water and Atmospheric ResearchWellingtonNew Zealand
  2. 2.Landcare ResearchAucklandNew Zealand

Personalised recommendations