Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-22T17:34:01.423Z Has data issue: false hasContentIssue false
  • English
  • Français

A new species of Cirrophorus (Annelida: Paraonidae) from Mediterranean organically enriched coastal environments, with taxonomic notes on the family

Published online by Cambridge University Press:  10 August 2017

Joachim Langeneck ,
Michele Barbieri ,
Ferruccio Maltagliati Open the ORCID record for Ferruccio Maltagliati [Opens in a new window]  and
Alberto Castelli
Joachim Langeneck*
Affiliation:
Department of Biology, University of Pisa, via Derna 1, 56126 Pisa, Italy
Michele Barbieri
Affiliation:
Department of Biology, University of Pisa, via Derna 1, 56126 Pisa, Italy
Ferruccio Maltagliati
Affiliation:
Department of Biology, University of Pisa, via Derna 1, 56126 Pisa, Italy
Alberto Castelli
Affiliation:
Department of Biology, University of Pisa, via Derna 1, 56126 Pisa, Italy
*
Correspondence should be addressed to: J. Langeneck, Department of Biology, University of Pisa, via Derna 1, 56126 Pisa, Italy email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Cirrophorus nikebianchii sp. nov. is described from brackish-water and organically enriched marine environments of the Mediterranean Sea. The new species is characterized by a very small prostomial antenna and a high number of branchiae pairs. A phylogenetic analysis carried out through the use of three molecular markers (16S rRNA, 18S rRNA and COI) supports the distinction between C. nikebianchii and C. furcatus, a closely related species with which it has been misidentified. Preliminary results obtained show that the genera Cirrophorus and Paradoneis are not reciprocally monophyletic, with uncertain relationships with the remaining genera of Paraonidae. This outcome suggests that the evolutionary history of Paraonidae is less straightforward than previously supposed. Moreover, the uncertainty about the taxonomic status of Paraonides neapolitana, type species of the genus Paraonides, makes the revamping of the taxonomy of Paraonidae more challenging. Awaiting support from studies including more species, and based on morphological and genetic data as well, we suggest to provisionally maintain the current use of Cirrophorus and Paradoneis, and to assign to Paraonella the species traditionally assigned to Paraonides.

Keywords

Paraonidaesystematicsbrackish-water environmentsmorphologyDNA sequencesphylogeny
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 97 , Special Issue 5: Proceedings of the 12th International Polychaete Conference Amgueddfa Cymru - National Museum Wales Cardiff, Wales, UK, 1-5 August 2016 , August 2017 , pp. 871 - 880
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Zoobank identifier: LSID urn:lsid:zoobank.org:pub:0B714E6D-D895-48D7-82C8-DE0EB3187F1F

References

REFERENCES

Aguirrezabalaga, F. and Gil, J. (2009) Paraonidae (Polychaeta) from the Capbreton Canyon (Bay of Biscay, NE Atlantic) with the description of eight new species. Scientia Marina 73, 631–666.Google Scholar
Akaike, H. (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.Google Scholar
Annenkova, N.P. (1934) Paraoniden der Meeren des Fernen Osten der USSR. Doklady Akademii Nauk SSSR 3, 656–658.Google Scholar
Blake, J.A. (1996) Family Paraonidae Cerruti, 1909. In Blake, J.A., Hilbig, B. and Scott, P.H. (eds) Taxonomic atlas of the benthic fauna of the Santa Maria Basin and Western Santa Barbara Channel. 6 – The Annelida Part 3. Polychaeta: Orbiniidae to Cossuridae. Santa Barbara, CA: Santa Barbara Museum of Natural History, pp. 27–70.Google Scholar
Blake, J.A. (2016) Paraonidae Cerruti, 1909. In Westheide, W. and Purschke, G. (eds) Handbook of zoology online, Annelida: polychaetes edition. Berlin: De Gruyter, pp. 6–52.Google Scholar
Bleidorn, C. (2005) Phylogenetic relationships and evolution of Orbiniidae (Annelida, Polychaeta) based on molecular data. Zoological Journal of the Linnean Society 144, 59–73.Google Scholar
Bonvicini Pagliai, A.M. and Cognetti, G. (1982) Ecology of polychaetes in the Orbetello lagoon (Tuscany). Bollettino di Zoologia 49, 51–60.Google Scholar
Cadman, P.S. and Nelson-Smith, A. (1990) Genetic evidence for two species of lugworm (Arenicola) in South Wales. Marine Ecology Progress Series 64, 107–112.Google Scholar
Carr, C.M., Hardy, S.M., Brown, T.M., Macdonald, T.A. and Hebert, P.D.N. (2011) A tri-oceanic perspective: DNA barcoding reveals geographic structure and cryptic diversity in Canadian polychaetes. PLoS ONE 6, e22232.Google Scholar
Castelli, A. (1985) Paraonidae (Annelida, Polychaeta) des fonds meubles infralittoraux des côtes toscanes. Cahiers de Biologie Marine 26, 267–279.Google Scholar
Castelli, A. (1987) Censimento dei policheti dei mari italiani: Paraonidae Cerruti, 1909. Atti della Società Toscana di Scienze Naturali, Memorie, Serie B 94, 319–340.Google Scholar
Castelli, A., Abbiati, M., Badalamenti, F., Bianchi, C.N., Cantone, G., Gambi, M.C., Giangrande, A., Gravina, M.F., Lanera, P., Lardicci, C., Somaschini, A. and Sordino, P. (1995) Annelida Polychaeta, Pogonophora, Echiura, Sipuncula. In Minelli, A., Ruffo, S. and La Posta, S. (eds) Checklist delle specie della fauna italiana. Bologna: Calderini, Volume 19, 45 pp.Google Scholar
Castelli, A. and Lardicci, C. (1985) Note preliminari allo studio dei Policheti della Baia di Portoferraio (Isola d'Elba). Oebalia 11, 763–766.Google Scholar
Cerruti, A. (1909) Contributo all'anatomia, biologia e sistematica delle Paraonidae (Levinsenidae), con particolare riguardo alle specie del golfo di Napoli. Mitteilungen aus der zoologischen Station zu Neapel 19, 459–512.Google Scholar
Chessa, L.A., Scardi, M., Serra, S., Pais, A., Lanera, P., Plastina, N., Valiante, L.M. and Vinci, D. (2007) Small-scale perturbation on soft bottom macrozoobenthos after mechanical cleaning operations in a Central-Western Mediterranean lagoon. Transitional Waters Bulletin 2, 9–19.Google Scholar
Çinar, M.E. and Dağli, E. (2013) Polychaetes (Annelida: Polychaeta) from the Aegean and Levantine coasts of Turkey, with descriptions of two new species. Journal of Natural History 47, 911–947.Google Scholar
Çinar, M.E., Dağli, E. and Açik, S. (2011) Annelids (Polychaeta and Oligochaeta) from the Sea of Marmara, with descriptions of five new species. Journal of Natural History 45, 2105–2143.Google Scholar
Çinar, M.E., Dağli, E. and Kurt Şahin, G. (2014) Checklist of the Annelida from the coasts of Turkey. Turkish Journal of Zoology 38, 734–764.Google Scholar
Como, S., Rossi, F. and Lardicci, C. (2004) Response of deposit-feeders to exclusion of epibenthic predators in a Mediterranean intertidal flat. Journal of Marine Biology and Ecology 303, 157–171.Google Scholar
Darriba, D., Taboada, G.L., Doallo, R. and Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.Google Scholar
Day, J.H. (1963) Polychaete Fauna of South Africa: Part 7. Species from depths between 1000 and 3330 meters west of Cape Town. Annals of the South African Museum 46, 353–371.Google Scholar
De Biasi, A.M. and Pacciardi, L. (2008) Macrobenthic communities in a fishery exclusion zone and in a trawled area of the middle Adriatic Sea (Italy). Ciencias Marinas 34, 433–444.CrossRefGoogle Scholar
de Léon-González, J.A. and Díaz-Castañeda, V. (2011) A new species of Paradoneis (Polychaeta: Paraonidae) from the western coast of Baja California, Mexico. Proceedings of the Biological Society of Washington 124, 40–44.Google Scholar
Ehlers, E. (1908) Die bodensässigen Anneliden aus den Sammlungen der deutschen Tiefsee-Expedition. Wissenschaftliche Ergebnisse der deutschen Tiefsee – Expedition auf dem Dampfer ‘Valdivia’ 1898–1899, 16, 1–168.Google Scholar
Fauvel, P. (1927) Polychètes sédentaires, Faune de France 16 edition. Paris: Lechevalier, 494 pp.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Gambi, M.C., Conti, G. and Bremec, C.S. (1998) Polychaete distribution, diversity and seasonality related to seagrass cover in shallow soft bottoms of the Tyrrhenian Sea (Italy). Scientia Marina 62, 1–17.Google Scholar
Glémarec, M. (1966) Paraonidae de Bretagne: description de Paradoneis armata nov. sp. Vie et Milieu, Ser. A 17, 1045–1052.Google Scholar
Grube, A.E. (1873) Über ein paar neue Anneliden aus der Familie der Spiodeen. Jahres-Bericht der Schlesichen Gesellschaft für vaterländische Cultur 50, 57–58.Google Scholar
Guindon, S. and Gascuel, O. (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology 52, 696–704.Google Scholar
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symposium Series 41, 95–98.Google Scholar
Hartman, O. (1957) Orbiniidae, Apistobranchidae, Paraonidae and Longosomidae. Allan Hancock Pacific Expeditions 15, 211–393.Google Scholar
Hartman, O. (1965) Deep-water benthic polychaetous annelids off New England to Bermuda and other North Atlantic areas. Occasional Papers of the Allan Hancock Foundation 28, 1–378.Google Scholar
Hartman, O. and Fauchald, K. (1971) Deep-water benthic polychaetous annelids off New England to Bermuda and other North Atlantic Areas. Part II. Allan Hancock Monographs in Marine Biology 6, 1–327.Google Scholar
Hartmann-Schröder, G. (1965) Die Polychaeten des Sublitorals. In Hartmann-Schröder, G. and Hartmann, G. (eds) Zur Kenntnis des Sublitorals der chilenischen Küste unter besonderer Berücksichtigung der Polychaeten und Ostracoden. (Mit bemerkungen über den Einfluss sauerstoffarmer Strömungen auf die Besiedlung von marinen Sedimenten.). Hamburg: Mitteilungen aus dem Hamburgischen zoologischen Museum und Institut, Volume 62, pp. 59–305.Google Scholar
Hobson, K.D. (1972) Two new species and two new records of the family Paraonidae (Annelida, Polychaeta) from the northeastern Pacific Ocean. Proceedings of the Biological Society of Washington 85, 549–556.Google Scholar
Imajima, M. (1973) Paraonidae (Polychaeta) from Japan. Bulletin of the National Scientific Museum of Tokyo 16, 253–292.Google Scholar
Katzmann, W. and Laubier, L. (1975) Paraonidae (Polychètes Sédentaires) de l'Adriatique. Annales der Naturhistorischen Museum in Wien 79, 567–588.Google Scholar
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J. and Higgins, D.G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.CrossRefGoogle ScholarPubMed
Laubier, L. (1966) Sur la présence du genre Cirrophorus (Polychètes, Paraonidae) en Méditerranée. Bulletin de la Société Zoologique de France 90, 469–477.Google Scholar
Laubier, L. (1967) Sur quelques Aricidea (Polychètes, Paraonidae) de Banyuls-sur-Mer. Vie et Milieu, Ser. A. 18, 99–132.Google Scholar
Laubier, L. and Ramos, J. (1974) Paraonidae (Polychètes Sédentaires) de Méditerranée. Bulletin du Muséum National d'Histoire Naturelle Ser. 3 168(Zool. 113), 1097–1148.Google Scholar
Levinsen, G.M.R. (1884) Systematisk-geografisk Oversigt over de nordiske Annulata, Gephyrea, Chaetognathi og Balanoglossi. Videnskabelige Meddelelser fra den naturhistoriske Forening i Kjöbenhavn 45, 92–350.Google Scholar
Lorenz, T.C. (2012) Polymerase chain reaction: basic protocol plus troubleshooting and optimization strategies. Journal of Visualized Experiments 63, e3998.Google Scholar
Mackie, A.S.Y. (1991) Paradoneis eliasoni sp. nov. (Polychaeta: Paraonidae) from northern European waters, with a redescription of Paradoneis lyra (Southern, 1914). In Petersen, M.E. and Kirkegaard, J.B. (eds) Systematics, biology and morphology of world Polychaeta. Proceedings of the 2nd International Polychaete Conference, Copenhagen, 1986. Ophelia Suppl. 5, 147–155.Google Scholar
Maggiore, F. and Keppel, E. (2007) Biodiversity and distribution of polychaetes and molluscs along the Dese estuary (Lagoon of Venice, Italy). Hydrobiologia 588, 189–203.Google Scholar
Maltagliati, F., Camilli, L., Lardicci, C. and Castelli, A. (2001) Evidence for morphological and genetic divergence in Perinereis cultrifera (Polychaeta: Nereididae) from two habitat types at Elba Island. Journal of the Marine Biological Association of the United Kingdom 81, 411–414.Google Scholar
Maltagliati, F., Casu, M. and Castelli, A. (2004) Morphological and genetic evidence supports the existence of two species in the genus Ophelia (Annelida, Polychaeta) from the Western Mediterranean. Biological Journal of the Linnean Society 83, 101–113.CrossRefGoogle Scholar
Maltagliati, F., Casu, M., Lai, T., Iraci Sareri, D., Casu, D., Curini-Galletti, M., Cantone, G. and Castelli, A. (2005) Taxonomic distinction of Ophelia barquii and O. bicornis (Annelida, Polychaeta) in the Mediterranean as revealed by ISSR markers and the number of nephridiopores. Journal of the Marine Biological Association of the United Kingdom 85, 835–841.Google Scholar
Medlin, L., Elwood, H.J., Stickel, S. and Sogin, M.L. (1988) The characterization of enzymatically amplified 16Slike rRNA-coding regions. Gene 71, 491–499.Google Scholar
Mesnil, F. (1897) Études de morphologie externe chez les Annélides. II. Remarques complémentaires sur les Spionidiens. La famille nouvelle des Disomidiens. La place des Aonides (sensu Tauber, Levinsen). Bulletin scientifique de la France et de la Belgique 30, 83–100, pl. 3.Google Scholar
Montesanto, G. (2015) A fast GNU method to draw accurate scientific illustrations for taxonomy. Zookeys 515, 191–206.Google Scholar
Nygren, A. and Pleijel, F. (2011) From one to ten in a single stroke – resolving the European Eumida sanguinea (Phyllodocidae, Annelida) species complex. Molecular Phylogenetics and Evolution 58, 132–141.Google Scholar
Örsted, A.S. (1843) Annulatorum danicorum conspectus. Volume Fasc. 1 Maricolae (Quaestio ab universitate Hafniensis ad solvendum proposita et proemio ornate). Hafniae (Copenhagen): Librariae Wahlianae, 52 pp.Google Scholar
Palumbi, S., Martin, A., Romano, S., McMillan, W.O., Stice, L. and Grabowski, G. (1991) The simple fool's guide to PCR, version 2.0. Honolulu: Department of Zoology and Kewalo Marine Laboratory, University of Hawaii.Google Scholar
Petroni, G., Dini, F., Verni, F. and Rosati, G. (2002) A molecular approach to the tangled intrageneric relationships underlying phylogeny in Euplotes (Ciliophora, Spirotrichea). Molecular Phylogenetics and Evolution 22, 118–130.Google Scholar
Reuscher, M.G. (2013) Cladistic analysis of the family Paraonidae (Annelida: Polychaeta) and the genera Cirrophorus and Paradoneis based on morphological characters. In Reuscher, M.G. (ed.) Biodiversity, ecology, and natural history of polychaetous annelids from the Gulf of Mexico. PhD thesis. Corpus Christi University, Corpus Christi, TX, pp. 192–237.Google Scholar
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. and Huelsenbeck, J.P. (2011) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.Google Scholar
Rossi, F. and Lardicci, C. (1995) Evoluzione delle comunità zoobentoniche di fondo molle della Laguna di Orbetello: variazioni nella composizione specifica. Atti della Società Toscana di Scienze Naturali, Memorie, Ser. B 102, 31–36.Google Scholar
Rouse, G.W. and Fauchald, K. (1997) Cladistics and polychaetes. Zoologica Scripta 26, 139–204.Google Scholar
Sardá, R., Gil, J., Taboada, S. and Gili, J.M. (2009) Polychaete species captured in sediment traps moored in northwestern Mediterranean submarine canyons. Zoological Journal of the Linnean Society 155, 1–21.Google Scholar
Schirosi, R., Musco, L. and Giangrande, A. (2010) Benthic assemblage of Acquatina Lake (South Adriatic Sea): present state and long-term faunistic changes. Scientia Marina 74, 235–246.Google Scholar
Simboura, N., Reizopoulou, S., Arvanitidis, C. and Basset, A. (2007) New information on the biogeographical and ecological distribution of Pionosyllis anophthalma Capaccioni & San Martín, 1989 (Polychaeta, Syllidae). Transitional Waters Bulletin 4, 53–58.Google Scholar
Simonini, R., Ansaloni, I., Bonini, P., Grandi, V., Graziosi, F., Iotti, M., Massamba N’Siala, G., Mauri, M., Montanari, G., Preti, M., De Nigris, N. and Prevedelli, D. (2007) Recolonization and recovery dynamics of the macrozoobenthos after sand extraction in relict sand bottoms of the Northern Adriatic Sea. Marine Environmental Research 64, 574–589.Google Scholar
Southern, R. (1914) Clare Island Survey. Archiannelida and Polychaeta. Proceedings of the Royal Irish Academy 31, 1–160.Google Scholar
Strelzov, V.E. (1968) Polychaete worms of the family Paraonidae (Polychaeta, Sedentaria) from the Barents Sea. Trudy Murmanskogo biologicheskogo instituta, Volume 17, 74–95. [In Russian]Google Scholar
Strelzov, V.E. (1973) Polychaete worms of the family Paraonidae Cerruti, 1909 (Polychaeta, Sedentaria). Moscow: Akademia Nauk, 170 pp. [In Russian]Google Scholar
Tauber, P. (1879) Annulata Danica. En kritisk revision af de in Danmark fundne Annulata Chaetognatha, Gephyrea, Balanoglossi, Discophoreae, Oligochaeta, Gymnocopa og Polychaeta. Copenhagen: Reitzel, 143 pp.Google Scholar
Webster, H.E. (1879) The Annelida Chaetopoda of the Virginian Coast. Transactions of the Albany Institute 9, 202–269.Google Scholar
Wu, B., Qian, P.-Y. and Zhang, S. (1991) Morphology, reproduction, ecology and allozyme electrophoresis of three Capitella sibling species in Qingdao (Polychaeta: Capitellidae). In Petersen, M.E. and Kirkegaard, J.B. (eds) Systematics, biology and morphology of world Polychaeta. Proceedings of the 2nd International Polychaete Conference, Copenhagen, 1986. Ophelia Suppl. 5, 391–400.Google Scholar
Zanol, J., Halanych, K.M. and Fauchald, K. (2014) Reconciling taxonomy and phylogeny in the bristleworm family Eunicidae (polychaete, Annelida). Zoologica Scripta 43, 79–100.Google Scholar