Register      Login
Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Cephalotrichella echinicola, sp. nov. (Palaeonemertea : Cephalotrichellidae), a new nemertean associated with sea urchins from Nha Trang Bay (South China Sea)

Alexei V. Chernyshev https://orcid.org/0000-0002-2203-3001 A B D , Neonila Polyakova A , Temir A. Britayev C , Olga A. Bratova C and Elena S. Mekhova C
+ Author Affiliations
- Author Affiliations

A National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok 690041, Russia.

B Far Eastern Federal University, Vladivostok 690600, Russia.

C AN Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninsky pr. 33, Moscow 129164, Russia.

D Corresponding author. Email: nemertea1969@gmail.com

Invertebrate Systematics 33(3) 518-529 https://doi.org/10.1071/IS18080
Submitted: 11 November 2018  Accepted: 29 December 2018   Published: 28 May 2019

Abstract

About 50 nemertean species have been reported to live in symbiotic relationships with other invertebrates, but only two hoplonemertean species are associated with echinoderms (starfish). The palaeonemertean Cephalotrichella echinicola, sp. nov. is described from samples collected in Nha Trang Bay, Vietnam, South China Sea. The species is the first known nemertean associated with sea urchins (Metalia sternalis and M. spatagus), living on both the oral and the aboral surfaces of the host and freely moving among its spines. The internal morphology of the new species is described based on histological sections and confocal laser scanning microscopy with phalloidin and antibody labelling. Sequences of three nuclear gene markers (18S rRNA, 28S rRNA, and histone H3) and two mitochondrial gene markers (16S rRNA and COI) were compared with those of other palaeonemertean species, and a phylogenetic analysis suggested that C. echinicola is closest to the free-living Cephalotrichella alba Gibson & Sundberg, 1992. Both the morphological data and the phylogenetic analysis provide additional evidence for distinguishing the families Cephalotrichidae and Cephalotrichellidae and support the rejection of Cephalotrichella as a junior synonym of Cephalothrix. A new diagnosis of the genus Cephalotrichella is given.

http://zoobank.org/urn:lsid:zoobank.org:pub:091B5D56-71B2-4F4C-9AD8-F666B4610DE2

Additional keywords: Nemertea, confocal microscopy, phylogenetic analysis, Metalia


References

Andrade, S. C. S., Strand, M., Schwartz, M., Chen, H.-X., Kajihara, H., von Döhren, J., Sun, S., Junoy, J., Thiel, M., Norenburg, J. L., Turbeville, J. M., Giribet, G., and Sundberg, P. (2012). Disentangling ribbon worm relationships: multi-locus analysis supports traditional classification of the phylum Nemertea. Cladistics 28, 141–159.
Disentangling ribbon worm relationships: multi-locus analysis supports traditional classification of the phylum Nemertea.Crossref | GoogleScholarGoogle Scholar |

Barel, C. D., and Kramers, P. G. (1977). A survey of the echinoderm associates of the north-east Atlantic area. Zoologische Verhandelingen Leiden 156, 1–159.

Beckers, P., Loesel, R., and Bartolomaeus, T. (2013). The nervous systems of basally branching Nemertea (Palaeonemertea). PLoS One 8, e66137.
The nervous systems of basally branching Nemertea (Palaeonemertea).Crossref | GoogleScholarGoogle Scholar | 23785478PubMed |

Berg, G., and Gibson, R. (1996). A redescription of Nemertoscolex parasiticus Greeff, 1879, an apparently endoparasitic heteronemertean from the coelomic fluid of the echiuroid Echiurus echiurus (Pallas). Journal of Natural History 30, 163–173.
A redescription of Nemertoscolex parasiticus Greeff, 1879, an apparently endoparasitic heteronemertean from the coelomic fluid of the echiuroid Echiurus echiurus (Pallas).Crossref | GoogleScholarGoogle Scholar |

Britayev, T. A., and Antokhina, T. I. (2012). Symbiotic polychaetes from Nhatrang Bay, Vietnam. In ‘Benthic Fauna of the Bay of Nhatrang, Southern Vietnam. Vol. 2’. (Eds T. A. Britayev, and D. S. Pavlov.) pp. 11–54. (KMK Press: Moscow.)

Britayev, T. A., Bratova, O. A., and Dgebuadze, P. Y. (2013). Symbiotic assemblage associated with the tropical sea urchin, Salmacis bicolor (Echinoidea: Temnopleuridae) in the An Thoi Archipelago, Vietnam. Symbiosis 61, 155–161.
Symbiotic assemblage associated with the tropical sea urchin, Salmacis bicolor (Echinoidea: Temnopleuridae) in the An Thoi Archipelago, Vietnam.Crossref | GoogleScholarGoogle Scholar |

Britayev, T. A., Bratova, O. A., Mekhova, E. S., and Chernyshev, A. V. (2018). The first record of symbiosis between palaeonemertean (Nemertea) and echinoderms (Echinodermata). Symbiosis , .
The first record of symbiosis between palaeonemertean (Nemertea) and echinoderms (Echinodermata).Crossref | GoogleScholarGoogle Scholar |

Bruce, A. J. (1982). The shrimps associated with Indo-West Pacific echinoderms, with the description of a new species in the genus Periclimenes Costa, 1844 (Crustacea: Pontoniinae). Australian Museum Memoir 16, 191–216.
The shrimps associated with Indo-West Pacific echinoderms, with the description of a new species in the genus Periclimenes Costa, 1844 (Crustacea: Pontoniinae).Crossref | GoogleScholarGoogle Scholar |

Bürger, O. (1895). Die Nemertinen des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. In ‘Fauna und Flora des Golfes von Neapel und der Angrenzenden Meeresabschnitte’. Series 22, pp. 1–743. (Verlag von R. Friedländer & Sohn: Berlin.)

Carus, J. V. (1885). ‘Prodromus faunae Mediterraneae sive descriptio animalium maris Mediterranei incolarum quam comparata silva rerum quatenus innotuit adiectis locis et nominibus vulgaribus eorumque auctoribus in commodum Zoologorum. Vol. I: Coelenterata, Echinodermata, Vermes, Arthropoda.’ (E. Schweizerbart’sche verlagshandlung (E. Koch): Stuttgart.) 524 pp.

Chen, H.-X., Strand, M., Norenburg, J. L., Sun, S.-C., Kajihara, H., Chernyshev, A. V., Maslakova, S. A., and Sundberg, P. (2010). Statistical parsimony networks and species assemblages in cephalotrichid nemerteans (Nemertea). PLoS One 5, e12885.
Statistical parsimony networks and species assemblages in cephalotrichid nemerteans (Nemertea).Crossref | GoogleScholarGoogle Scholar |

Chernyshev, A. V. (1991). Tetrastemma commensalis and Asteronemertes gibsoni gen. et sp. n. (Hoplonemertini, Tetrastemmidae) – commensals of the starfish. Зоологический журнал 70, 34–39.

Chernyshev, A. V. (1998). Nemerteans of the genus Tetrastemma (Enopla, Monostilifera) from the Far East seas of Russia. Зоологический журнал 77, 995–1002.

Chernyshev, A. V. (2011). ‘Comparative Morphology, Systematics and Phylogeny of the Nemerteans.’ (Dalnauka: Vladivostok.) [In Russian.]

Chernyshev, A. V. (2014). Nemertean biodiversity in the Sea of Japan and adjacent areas. In ‘Marine Biodiversity and Ecosystem Dynamics of the North-Western Pacific Ocean’. (Eds S. Sun, A.V. Adrianov, K.A. Lutaenko, X.-X. Sun .) pp. 119–135. (Publishing House of Science: Beijing.)

Chernyshev, A. V. (2015). CLSM analysis of the phalloidin-stained muscle system of the nemertean proboscis and rhynchocoel. Zoological Science 32, 547–560.
CLSM analysis of the phalloidin-stained muscle system of the nemertean proboscis and rhynchocoel.Crossref | GoogleScholarGoogle Scholar | 26654037PubMed |

Chernyshev, A. V. (2016). Nemerteans of the coastal waters of Vietnam. In ‘Biodiversity of the Western Part of the South China Sea’. (Eds A. V. Adrianov, and K. A. Lutaenko.) pp. 279–314. (Dalnauka: Vladivostok.)

Chernyshev, A. V., and Magarlamov, T. Yu. (2013). Metameric structures in the subepidermal nervous system of the nemerteans with review of the metamerism in Nemertea. Invertebrate Zoology 10, 245–254.
Metameric structures in the subepidermal nervous system of the nemerteans with review of the metamerism in Nemertea.Crossref | GoogleScholarGoogle Scholar |

Coe, W. R. (1902). The nemertean parasites of crabs. American Naturalist 36, 431–450.
The nemertean parasites of crabs.Crossref | GoogleScholarGoogle Scholar |

Colgan, D. J., McLauchlan, A., Wilson, G. D. F., Livingston, S. P., Edgecombe, G. D., Macaranas, J., Cassis, G., and Gray, M. R. (1998). Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Australian Journal of Zoology 46, 419–437.
Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution.Crossref | GoogleScholarGoogle Scholar |

Coppard, S. E., and Campbell, A. C. (2004). Organisms associated with diadematid echinoids in Fiji. In ‘Echinoderms: München’. (Eds T. Heinzeller, and J. H. Nebelsick.) pp. 171–176. (Taylor and Francis: London.)

Dieck, G. (1874). Beiträge zur Entwickelungsgeschichte der Nemertinen. Jenaische Zeitschrift für Naturwissenschaft 8, 500–521.

Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. C. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 7881515PubMed |

Gibson, R. (1974). A new species of commensal hoplonemertean from Australia. Zoological Journal of the Linnean Society 55, 247–266.
A new species of commensal hoplonemertean from Australia.Crossref | GoogleScholarGoogle Scholar |

Gibson, R. (1986). Redescription and taxonomic reappraisal of Nemertopsis actinophila Bürger, 1904 (Nemertea: Hoplonemertea: Monostilifera). Bulletin of Marine Science 39, 42–60.

Gibson, R., and Sundberg, P. (1992). Three new nemerteans from Hong Kong. In ‘The Marine Flora and Fauna of Hong Kong and Southern China III, V. 1’. (Ed. B. Morton.) pp. 97–129. (University Press: Hong Kong.)

Giribet, G., Carranza, S., Baguna, J., Riutort, M., and Ribera, C. (1996). First molecular evidence for the existence of a Tardigrada+Arthropoda clade. Molecular Biology and Evolution 13, 76–84.
First molecular evidence for the existence of a Tardigrada+Arthropoda clade.Crossref | GoogleScholarGoogle Scholar | 8583909PubMed |

Giribet, G., Distel, D. L., Polz, M., Sterrer, W., and Wheeler, W. C. (2000). Triploblastic relationships with emphasis on the acoelomates and the position of Gnathostomulida, Cycliophora, Plathelminthes, and Chaetognatha: a combined approach of 18S rDNA sequences and morphology. Systematic Biology 49, 539–562.
Triploblastic relationships with emphasis on the acoelomates and the position of Gnathostomulida, Cycliophora, Plathelminthes, and Chaetognatha: a combined approach of 18S rDNA sequences and morphology.Crossref | GoogleScholarGoogle Scholar | 12116426PubMed |

Giribet, G., Okusu, A., Lindgren, A. R., Huff, S. W., Schrödl, M., and Nishiguchi, M. K. (2006). Evidence for a clade composed of molluscs with serially repeated structures: monoplacophorans are related to chitons. Proceedings of the National Academy of Sciences of the United States of America 103, 7723–7728.
Evidence for a clade composed of molluscs with serially repeated structures: monoplacophorans are related to chitons.Crossref | GoogleScholarGoogle Scholar | 16675549PubMed |

Hayes, F. E. (2007). Decapod crustaceans associating with the sea urchin Diadema antillarum in the Virgin Islands. Nauplius 15, 81–85.

Hubrecht, A. A. W. (1879). The genera of European nemerteans critically revised, with description of several new species. Notes Leyden Museum 1, 193–232.

Ivanov, V., Bigatti, G., Penchaszadeh, P., and Norenburg, J. L. (2002). Malacobdella arrokeana (Nemertea: Bdellonemertea), a new species of nemertean from the southwestern Atlantic Ocean entocommensal in Panopea abbreviata (Bivalvia, Heterodonta, Hiatellidae) in Argentina. Proceedings of the Biological Society of Washington 115, 359–367.

Iwata, F. (1967). Uchidana parasita nov. gen. et nov. sp., a new parasitic nemertean from Japan with peculiar morphological characters. Zoologischer Anzeiger 178, 122–136.

Jangoux, M. (1987a). Diseases of Echinodermata. II. Agents metazoans (Mesozoa to Bryozoa). Diseases of Aquatic Organisms 2, 205–234.
Diseases of Echinodermata. II. Agents metazoans (Mesozoa to Bryozoa).Crossref | GoogleScholarGoogle Scholar |

Jangoux, M. (1987a). Diseases of Echinodermata. III. Agents metazoans (Annelida to Pisces). Diseases of Aquatic Organisms 3, 59–83.
Diseases of Echinodermata. III. Agents metazoans (Annelida to Pisces).Crossref | GoogleScholarGoogle Scholar |

Jensen, K., and Sadeghian, P. S. (2005). Nemertea (ribbon worms). In ‘Marine Parasitology’. (Ed. K. Rohde.) p. 592. (CSIRO Publishing: Melbourne.)

Junoy, J., Andrade, S. C. S., and Giribet, G. (2010). Phylogenetic placement of a new hoplonemertean species commensal on ascidians. Invertebrate Systematics 24, 616–629.
Phylogenetic placement of a new hoplonemertean species commensal on ascidians.Crossref | GoogleScholarGoogle Scholar |

Kajihara, H. (2006). Four palaeonemerteans (Nemertea: Anopla) from a tidal flat in middle Honshu, Japan. Zootaxa 1163, 1–47.

Kajihara, H. (2007). Two species of Nemertopsis (Nemertea: Hoplonemertea: Monostilifera) living in association with Capitulum mitella (Crustacea: Cirripedia: Thoracica: Lepadomorpha). Zootaxa 1446, 43–58.

Kajihara, H., and Kuris, A. (2013). Ovicides paralithodis (Nemertea, Carcinonemertidae), a new species of symbiotic egg predator of the red king crab Paralithodes camtschaticus (Tilesius, 1815) (Decapoda, Anomura). Zookeys 258, 1–15.

Kyao, N. N. (1954). A new species of nemerteans, Amphiporus commensalis sp. n., from ambulacral grooves of the starfish Crossaster papposus. Uchenye zapiski Leningradskogo Universiteta. Seriya Biologicheskich Nauk 35, 135–139.

Kajihara, H., Chernyshev, A. V., Sun, S., Sundberg, P., and Crandall, F. B. (2008). Checklist of nemertean genera and species (Nemertea) published between 1995 and 2007. Species Diversity 13, 245–274.
Checklist of nemertean genera and species (Nemertea) published between 1995 and 2007.Crossref | GoogleScholarGoogle Scholar |

Kvist, S., Laumer, C. E., Junoy, J., and Giribet, G. (2014). New insights into the phylogeny, systematics and DNA barcoding of Nemertea. Invertebrate Systematics 28, 287–308.
New insights into the phylogeny, systematics and DNA barcoding of Nemertea.Crossref | GoogleScholarGoogle Scholar |

Kvist, S., Chernyshev, A. V., and Giribet, G. (2015). Phylogeny of Nemertea with special interest in the placement of diversity from Far East Russia and northeast Asia. Hydrobiologia 760, 105–119.
Phylogeny of Nemertea with special interest in the placement of diversity from Far East Russia and northeast Asia.Crossref | GoogleScholarGoogle Scholar |

Lanfear, R., Calcott, B., Ho, S. Y. W., and Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 22319168PubMed |

Lanfear, R., Calcott, B., Kainer, D., Mayer, C., and Stamatakis, A. (2014). Selecting optimal partitioning schemes for phylogenomic datasets. BMC Evolutionary Biology 14, 82.
Selecting optimal partitioning schemes for phylogenomic datasets.Crossref | GoogleScholarGoogle Scholar | 24742000PubMed |

Leasi, F., and Norenburg, J. L. (2014). The necessity of DNA taxonomy to reveal cryptic diversity and spatial distribution of meiofauna, with a focus on Nemertea. PLoS One 9, e104385.
The necessity of DNA taxonomy to reveal cryptic diversity and spatial distribution of meiofauna, with a focus on Nemertea.Crossref | GoogleScholarGoogle Scholar | 25093815PubMed |

Littlewood, D. T. J. (1994). Molecular phylogenetics of cupped oysters based on partial 28S rRNA gene sequences. Molecular Phylogenetics and Evolution 3, 221–229.

Magarlamov, T. Y., Chernyshev, A. V., and Turbeville, J. M. (2018). Pseudocnidae of archinemerteans (Nemertea, Palaeonemertea) and their implications for nemertean systematics. Journal of Morphology 279, 1444–1454.
Pseudocnidae of archinemerteans (Nemertea, Palaeonemertea) and their implications for nemertean systematics.Crossref | GoogleScholarGoogle Scholar | 30184245PubMed |

Noren, M., and Jondelius, U. (1999). Phylogeny of the Prolecithophora (Platyhelminthes) inferred from 18S rDNA Sequences. Cladistics 15, 103–112.
Phylogeny of the Prolecithophora (Platyhelminthes) inferred from 18S rDNA Sequences.Crossref | GoogleScholarGoogle Scholar |

Norenburg, J., Gibson, R., Herrera Bachiller, A., and Strand, M. (2018). Cephalotrichella Wijnhoff, 1913. WORMS: World Register of Marine Species. Available at: http://www.marinespecies.org/aphia.php?p=taxdetails&id=122380 [accessed 23 September 2018].

Palumbi, S., Martin, A., Romano, S., McMillan, W. O., Stice, L., and Grabowski, G. (1991). ‘The Simple Fools Guide to PCR.’ Ver. 2.0. (Department of Zoology and Kewalo Marine Laboratory, University of Hawaii: Honolulu, HI.)

Rambaut, A., Drummond, A. J., Xie, D., Baele, G., and Suchard, M. A. (2018). Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67, 901–904.
Posterior summarisation in Bayesian phylogenetics using Tracer 1.7.Crossref | GoogleScholarGoogle Scholar | 29718447PubMed |

Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar | 22357727PubMed |

Sadeghian, P., and Santos, C. (2010). Two new species of Carcinonemertes (Hoplonemertea: Carcinonemertidae) living in association with leucosiid crabs from California and Tasmania. Journal of Natural History 44, 2395–2409.
Two new species of Carcinonemertes (Hoplonemertea: Carcinonemertidae) living in association with leucosiid crabs from California and Tasmania.Crossref | GoogleScholarGoogle Scholar |

Senz, W. (2000). Neue Nemertinen aus dem Golf von Arabien. 1. Palaeonemertini. Annalen des Naturhistorischen Museums in Wien 102B, 321–373.

Shields, J. D., and Segonzac, M. (2007). New nemertean worms (Carcinonemertidae) on bythograeid crabs (Decapoda: Brachyura) from Pacific hydrothermal vent sites. Journal of Crustacean Biology 27, 681–692.

Simpson, L. A., Ambrosio, L. J., and Baeza, J. A. (2017). A new species of Carcinonemertes, Carcinonemertes conanobrieni sp. nov. (Nemertea: Carcinonemertidae), an egg predator of the Caribbean spiny lobster, Panulirus argus. PLoS One 12, e0177021.
A new species of Carcinonemertes, Carcinonemertes conanobrieni sp. nov. (Nemertea: Carcinonemertidae), an egg predator of the Caribbean spiny lobster, Panulirus argus.Crossref | GoogleScholarGoogle Scholar | 28475595PubMed |

Sundberg, P., Gibson, R., and Olsson, U. (2003). Phylogenetic analysis of a group of palaeonemerteans (Nemertea) including two new species from Queensland and the Great Barrier Reef, Australia. Zoologica Scripta 32, 279–296.
Phylogenetic analysis of a group of palaeonemerteans (Nemertea) including two new species from Queensland and the Great Barrier Reef, Australia.Crossref | GoogleScholarGoogle Scholar |

Sundberg, P., Chernyshev, A. V., Kajihara, H., Kånneby, T., and Strand, M. (2009). Character-matrix based descriptions of two new nemertean (Nemertea) species. Zoological Journal of the Linnean Society 157, 264–294.
Character-matrix based descriptions of two new nemertean (Nemertea) species.Crossref | GoogleScholarGoogle Scholar |

Sundberg, P., Kvist, S., and Strand, M. (2016). Evaluating the utility of single-locus DNA barcoding for the identification of ribbon worms (phylum Nemertea). PLoS One 11, e0155541.
Evaluating the utility of single-locus DNA barcoding for the identification of ribbon worms (phylum Nemertea).Crossref | GoogleScholarGoogle Scholar | 27171471PubMed |

Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution 30, 2725–2729.
MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0.Crossref | GoogleScholarGoogle Scholar | 24132122PubMed |

Vaidya, G., Lohman, D. J., and Meier, R. (2011). SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27, 171–180.
SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information.Crossref | GoogleScholarGoogle Scholar |

Venmathi Maran, B. A. V., Kim, I.-H., Bratova, O. A., and Ivanenko, V. N. (2017). Two new species of poecilostomatoid copepods symbiotic on the venomous echinoid Toxopneustes pileolus (Lamarck) (Echinodermata) from Vietnam. Systematic Parasitology 94, 227–241.
Two new species of poecilostomatoid copepods symbiotic on the venomous echinoid Toxopneustes pileolus (Lamarck) (Echinodermata) from Vietnam.Crossref | GoogleScholarGoogle Scholar |

Whiting, M. F., Carpenter, J. M., Wheeler, Q. D., and Wheeler, W. C. (1997). The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology 46, 1–68.
| 11975347PubMed |

Wijnhoff, G. (1913). Die Gattung Cephalothrix und ihre Bedeutung für die Systematik der Nemertinen. II. Systematischer Teil. Zoologische Jahrbucher. Abteilung fur Systematik, Geographie und Biologie der Tiere 34, 291–320.
Die Gattung Cephalothrix und ihre Bedeutung für die Systematik der Nemertinen. II. Systematischer Teil.Crossref | GoogleScholarGoogle Scholar |