Abstract
A large collection of mesoparasitic copepods from polychaete hosts collected in northern European waters was examined. The term mesoparasitic refers to highly transformed copepods where the adult female attaches by embedding part of its body in the host. Representatives of five known familes were found and a new family is established. A single new species, Bradophila minuta sp. nov., was described in the family Bradophilidae. It occurred exclusively on the flabelligerid Diplocirus glaucus (Malmgren, 1867). Two genera of the family Herpyllobiidae were represented: Herpyllobius Steenstrup & Lütken, 1861 and Eurysilenium M. Sars, 1870. Herpyllobius arcticus Steenstrup & Lütken, 1861 was found on at least five different polynoid hosts, two of which, Harmothoe fragilis Moore, 1910 and Antinoe sp., were new host records. A new species, H. cluthensis sp. nov. was described from Malmgrenia species in Scottish waters. The large species, Herpyllobius cordiformis Lützen, 1964, was collected in Arctic waters from Eunoe cf. oerstedi. It is the first report of this parasite in Europe. The common parasite H. polynoes (Krøyer, 1864) was found on six different polynoid hosts, three of which, Harmothoe bifera, Malmgreniella mcintoshi Tebble & Chambers, 1982 and Eunoe ?barbata are new host records. Eurysilenium truncatum M. Sars, 1870 was collected from Eucranta villosa Malmgren, 1866, Eunone sp., and Gattyana cirrhosa (Pallas, 1766). The material from Eucranta villosa caught at 72.6ºN comprises both a new host record and is the most northerly report of this parasite. Specimens of Eurysilenium which differed from E. truncatum in a number of features were found on Harmothoe fragilis and H. impar (Johnston, 1839). A new family, the Pholoicolidae, is established to accommodate Pholicola chambersae gen. et sp. nov., parasitic on Pholoe pallida Chambers, 1985. The family Phyllodicolidae was represented by all three of its known species: Phyllodicola petiti (Delamare Deboutteville & Laubier, 1960), Cyclorhiza eteonicola Heegaard, 1942 and C. megalova Gotto & Leahy, 1988. The former was found on Eumida ockelmanni Eibye-Jacobsen, 1987, a new host record. A single ovigerous female of C. eteonicola was collected from a new host, Eteone spetsbergensis Malmgren, 1865. Cyclorhiza megalova was common on Eteone longa (Fabricius, 1780) and E. longa/flava complex. A rich diversity of members of the family Saccopsidae was found, including three known species of Melinnacheres M. Sars, 1870 plus nine new species placed in four new genera. Melinnacheres was represented by M. ergasiloides M. Sars, 1870, M. steenstrupi Bresciani & Lützen, 1961 and M. terebellidis Levinsen, 1878. Melinnacheres ergasiloides was found on Melinna elizabethae McIntosh, 1914, M. steenstrupi on members of the Terebellides stroemi-complex and T. atlantis Williams, 1984, while M. terebellidis was found on the T. stroemi-complex and on T. shetlandica Parapar, Moreira & O'Reilly, 2016. A new genus, Trichobranchicola gen. nov., was established to accommodate T. antennatus gen. et sp. nov., a parasite of Trichobranchus sikorskii Leontovich & Jirkov in Jirkov, 2001, T. glacialis Malmgren, 1866 and Trichobranchus sp. The second new genus, Lanassicola gen. nov., was established to accommodate the type species, Lanassicola arcticus gen. et sp. nov. parasitic on Lanassa venusta (Malm, 1874), plus two additional species, L. bilobatus gen. et sp. nov. on Lanassa nordenskjoeldi Malmgren, 1866, and L. dorsilobatus gen. et sp. nov. on Proclea graffii (Langerhans, 1884). A new subfamily, Euchonicolinae, was established within the Saccopsidae to accommodate two new genera, Euchonicola gen. nov. and Euchonicoloides gen. nov. The type species of Euchonicola gen. nov. is E. caudatus gen. et sp. nov., a parasite of Euchone sp., and it includes two other species, E. linearis gen. et sp. nov. on Chone sp., and E. parvus gen. et sp. nov. on Euchone sp. The type species of Euchonicoloides gen. nov. is E. elongatus gen. et sp. nov. found on a host belonging to the genus Euchone, and it also includes Euchonicoloides halli gen. et sp. nov. from Jasmineira caudata Langerhans, 1880. Four species of the family Xenocoelomidae were found: Xenocoeloma alleni (Brumpt, 1897), X. brumpti Caullery & Mesnil, 1915, X. orbicularis sp. nov. and Aphanodomus terebellae (Levinsen, 1878). Xenocoeloma alleni was found on four different species of Polycirrus and on Amaeana trilobata (M. Sars, 1863) and X. brumpti was found on Polycirrus norvegicus Wollebaek, 1912. Xenocoeloma orbicularis sp. nov. occurred only on Paramphitrite birulai (Ssolowiew, 1899). Aphanodomus terebellae was found on three hosts, only one of which, Leaena abranchiata was new.
References
Barnich, R., Dietrich, A., Hager, T. & Fiege, D. (2017) On the genera Malmgrenia McIntosh, 1874 and Pettibonesia Nemésio, 2006 in the Northeast Atlantic and Mediterranean Sea, with descriptions of two new species. Marine Biodiversity.
https://doi.org/10.1007/s12526-017-0802-4Bocquet, C., Bocquet-Védrine, J. & L’Hardy, J.P. (1965) Sur la redécouverte, a Roscoff, de Xenocoeloma alleni (Brumpt) et sur l’existence d’un tegument propre, indépendant de celui de l’hôte: Polycirrus caliendrum Claparède chez ce copépode parasite. Bulletin du Muséum national d’Histoire naturelle, Series 2, 36, 622–625.
Bocquet, C., Bocquet-Védrine, J. & L’Hardy, J.P. (1968) Analyse des rapports du copépode parasite Xenocoeloma alleni (Brumpt) et de son hôte Polycirrus caliendrum Claparède. Cahiers de Biologie Marine, 9, 285–296.
https://doi.org/10.21411/CBM.A.EC8D8C4
Bocquet, C., Bocquet-Védrine, J. & L’Hardy, J.P. (1970) Contribution à l’étude du développement des organes génitaux chez Xenocoeloma alleni (Brumpt), Copépode parasite de Polycirrus caliendrum Claparède. Cahiers de Biologie Marine, 11 (2), 195–208.
Boxshall, G.A. (1977) On the synonymy of the genera Oestrella McIntosh, 1885, and Melinnacheres M.Sars, 1870 (Copepoda). Crustaceana, 32, 214–215.
https://doi.org/10.1163/156854077X00647
Boxshall, G.A. & Halsey, S.H. (2004) An Introduction to Copepod Diversity. The Ray Society, London, 966 pp.
Boxshall, G.A., O’Reilly, M., Sikorski, A. & Summerfield, R. (2015) A new genus and family of copepods parasitic on polychaetes of the genus Jasmineira Langerhans, 1880 (family Sabellidae) in the northeastern Atlantic. Zootaxa, 4018 (3), 426–436.
https://doi.org/10.11646/zootaxa.4018.3.6Bresciani, J. & Lützen, J. (1961) The anatomy of a parasitic copepod, Saccopsis steenstrupi n. sp. Crustaceana, 3, 9–23.
https://doi.org/10.1163/156854061X00491
Bresciani, J. & Lützen, J. (1966) The anatomy of Aphanodomus terebellae (Levinsen) with remarks on the sexuality of the family Xenocoelomidae nov. fam. (Parasitic Copepoda). Bulletin du Muséum national d’Histoire naturelle, Série 2, 37 (5), 787–806.
Bresciani, J. & Lützen, J. (1972) The sexuality of Aphanodomus (parasitic copepod) and the phenomenon of cryptogonochorism. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening I Kjøbenhavn, 135, 7–20.
Bresciani, J. & Lützen, J. (1974) On the biology and development of Aphanodomus Wilson (Xenocoelomidae), a parasitic copepod of the polychaete Thelepus cincinnatus. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening I Kjøbenhavn, 137, 25–63.
Bresciani, J. & Lützen, J. (1975) Melinnacheres ergasiloides M. Sars, a parasitic copepod of the polychaete Melinna cristata, with notes on multiple infections caused by annelidicolous copepods. Ophelia, 13, 31–42.
https://doi.org/10.1080/00785326.1974.10430590
Brumpt, E. (1897) Sur un Copépode nouveau (Saccopsis Alleni, nova species, parasite de Polycirrus aurantiacus Grube). Compte Rendu Hebdomadaire des Séances de l’Académie des Sciences, Paris, 124, 1464–1467.
Burmeister, H. (1834) Beiträge zur Naturgeschichte der Rankenfüsser (Cirripedia). G. Reimer, Berlin, 60 pp., taf. 1–2.
Caullery, M. & Mesnil, F. (1915) Sur la structure d'un Copépode parasite (Xenocoeloma brumpti, n. g., n. sp.) et ses rapports avec son hôte (Polycirrus arenivorus Caull.). Compte Rendu Hebdomadaire des Séances de l’Académie des Sciences, Paris, 161 (23), 709–712.
Caullery, M. & Mesnil, F. (1919) Xenocoeloma brumpti C. et M., Copépode parasite de Polycirrus arenivorus C. Bulletin Biologique de la France at de la Belgique, 53, 161–233, 4 pls.
Chambers, S.J. & Muir, A.I. (1997) Polychaetes: British Chrysopetaloidea, Pisionoidea and Aphroditoidea. Synopses of the British Fauna, New Series, No. 54, 1–202.
Cochrane, S.J. (2003) Snowflakes and feather-dusters—some challenges for soft bottom fanworm systematics. Hydrobiologia, 496, 49–62.
https://doi.org/10.1023/A:1026168025573
Delamare Deboutteville, C. & Laubier, L. (1960a) Les Phyllocolidae, une famille nouvelle de Copépodes parasites d'Annélides Polychètes. Compte Rendu Hebdomadaire des Séances de l’Académie des Sciences, Paris, 251 (19), 2083–2085.
Delamare Deboutteville, C. & Laubier, L. (1960b) Les Phyllocolidae Delamare et Laubier, Copépodes parasites d'Annélides Polychètes Phyllodocides, et leur rapports avec les Copépodes annélidicoles. Compte Rendu Hebdomadaire des Séances de l’Académie des Sciences, Paris, 251 (20), 2231–2233.
Delamare Deboutteville, C. & Laubier, L. (1961) Note recticative. Vie et Milieu, 11, 690.
Giangrande, A., Wasson, B., Lezzi, M. & Licciano, M. (2017) Description of Euchone anceps sp. nov. (Annelida: Sabellidae) from the Mediterranean Sea and Northeast Atlantic, with remarks on the difficulty of generic definition. The European Zoological Journal, 84 (1), 193–207.
https://doi.org/10.1080/24750263.2017.1297499
Glasby, C.J. & Hutchings, P. (2014) Revision of the taxonomy of Polycirrus Grube, 1850 (Annelida, Terebellida, Polycirridae). Zootaxa, 3877 (1), 1–117.
https://doi.org/10.11646/zootaxa.3877.1.1
Gotto, V. (1993) Commensal and Parasitic Copepods associated with Marine Invertebrates (and whales). Synopses of the British Fauna, New Series, No. 46, 1–350.
Gotto, R.V. & Leahy, Y. (1988) A new annelidicolous copepod, Cyclorhiza megalova n. sp., with comments on its functional biology and possible phylogenetic relationship. Hydrobiologia, 167/168, 533–538, figs. 1–3.
https://doi.org/10.1007/BF00026348
Gotto, R.V. & O’Connor, B.Y. (1980) Some annelidicolous copepods from the West coast of Ireland. Irish Naturalists’ Journal, 20 (3), 109–113.
Gravier, C. (1912a) Sur un nouveau genre de Crustacé parasite d'un Syllidien de l'Antarctique sud-américaine (Thylacoides nov. g. sarsi n. sp.). Bulletin du Muséum national d’Histoire naturelle Paris, 18, 71–74.
Gravier, C. (1912b) Sur quelques Crustacés parasites annélidicoles provenant de la seconde expédition antarctique française. Compte Rendu Hebdomadaire des Séances de l’Académie des Sciences, Paris, 154 (13), 830–832.
Gravier, C. (1913) Crustacés parasites d'annelides polychaetes. In: Deuxième Expédition Antarctique Francaise (1908–1910), pp. 27–77, figs. A–B, 1–60.
Gravier, C. (1918) Contribution à l'étude d'un Copépode (Flabellicola neapolitana Gravier) parasite d'un Annélide Polychète (Flabelligera (Siphonostoma) diplochaitos (Otto)). Pubblicazione Stazione Zoologica Napoli, 2, 209–222, pl. 2.
Hansen, H.J. (1892) Rhizorhina Ampeliscae n. gen., n. sp. en ny til Herpyllobiidae n. fam. horende Copepod, snyltende paa Amp. laevigata Lilljeb. Entomologiske Meddelelser, 3, 207–234, pl. 3.
Hansen, H.J. (1900) Danmarks Stilling og Tilstand, II, Det Kongelige Danske Videnskabernes Selskab med Tillaeg: Rhizorhina, Herpyllobius og Søren Jensen. Kjøbenhavn, 200 pp.
Heegaard, P.E. (1942) Cyclorhiza eteonicola n. gen., n. sp., a new parasitic copepod. Kongelige Norske Videnskabernes Selskabs Forhandlinger, 15 (14), 53–54.
Huys, R. (2016) Enigmas from the past: M’Intosh’s (1885) annelidicolous copepods from the voyage of H.M.S. Challenger. Zootaxa, 4174 (1), 355–385.
https://doi.org/10.11646/zootaxa.4174.1.22
Huys, R. & Boxshall, G.A. (1991) Copepod Evolution. The Ray Society, London, 468 pp.
Jensen, S. (1900) Nogle oplysninger om Rhizorhina ampeliscae H.J.H., Herpyllobius arcticus Stp.-Ltk. og Fam. Herpyllobiidae H.J.H. Oversigt over det Kongelige Danske Videnskabernes Selskabs Forhandlinger, 1900, 61–112.
Kim, I.-H., Sikorski, A., O’Reilly, M. & Boxshall, G.A. (2013) Copepods associated with polychaete worms in European seas. Zootaxa, 3651 (1), 1–62.
https://doi.org/10.11646/zootaxa.3651.1.1
Krøyer, H. (1864) Bidrag til Kundskab om Snyltekrebsene. Naturhistorisk Tidsskrift, Series 3, 2 (3), 321–426, pls 10–18.
Laubier, L. (1961) Phyllodicola petiti (Delamare et Laubier, 1960) et la famille des Phyllodicolidae, Copépodes parasites d’Annélides Polychètes en Méditerranée occidentale. Crustaceana, 2, 228–242.
https://doi.org/10.1163/156854061X00202
Leigh-Sharpe, W.H. (1926) The Herpyllobiidae. A family of Copepoda parasitic on polynoid worms. Parasitology, Cambridge, 18 (3), 269–276.
https://doi.org/10.1017/S0031182000005254
Levinsen, G.M.R. (1878) Om nogle parasitiske Krebsdyr, der snylte hos Annelider. Videnskalbelige Meddelelser fra dansk Naturhistorisk Forening I Kjøbenhavn, 1877–78, 351–380, pl. 6.
López-González, P.J. & Bresciani, J. (2001) New Antarctic records of Herpyllobius Steenstrup & Lütken, 1861 (parasitic Copepoda) from the EASIZ-III cruise, with description of two new species. Scientia Marina, 65, 357–366.
https://doi.org/10.3989/scimar.2001.65n4357
López-González, P.J., Bresciani, J. & Conradi, M. (2000) Two new species of Herpyllobius Steenstrup & Lütken, 1861 and a new record of Herpyllobius antarcticus Vanhöffen, 1913 (parasitic Copepoda) from the Weddell Sea, Antarctica. Polar Biology, 23, 265–271.
https://doi.org/10.1007/s003000050443
López-González, P.J., Bresciani, J. & Conradi, M. (2006) New genus, three new species and new records of Herpyllobiidae Hansen, 1892 (Crustacea, Copepoda), parasites of polychaetes from Antarctica. Scientia Marina, 70, 243–259.
https://doi.org/10.3989/scimar.2006.70n2243.
Lützen, J. (1964a) A revision of the family Herpyllobiidae, (parasitic copepods) with notes on hosts and distribution. Ophelia, 1, 241–274.
https://doi.org/10.1080/00785326.1964.10416282
Lützen, J. (1964b) Parasitic copepods from marine polychaetes of eastern North America. Naturaliste Canadian, 91, 255–267.
Lützen, J. (1966) The anatomy of the family Herpyllobiidae (parasitic copepods). Ophelia, 3, 45–64, pl. 1.
https://doi.org/10.1080/00785326.1966.10409632
Lützen, J. (1968) On the biology of the family Herpyllobiidae (parasitic copepods). Ophelia, 5, 175–187.
https://doi.org/10.1080/00785326.1968.10409630
Lützen, J. & Jones, J.B. (1976) Two new species of Herpyllobius (parasitic Copepoda) from New Zealand and the Antarctic. New Zealand Journal of Marine and Freshwater Research, 10, 371–374.
https://doi.org/10.1080/00288330.1976.9515620
Marchenkov, A.V. (1999) Symbiotic and parasitic Crustacea off benthic marine invertebrates from the Arctic Seas of Russia. Unpublished PhD thesis, Zoological Institute, Russian Academy of Sciences, Saint Petersburg, 193 pp.
Marchenkov, A.V. (2002) Bradophilidae fam. nov.—the new family of mesoparasitic copepod collected from the polychaete Brada villosa from the White Sea. Parazitologiya, 36 (6), 514–516.
M’Intosh, W.C. (1885) Report on the Annelida Polychaeta collected by H.M.S. Challenger during the years 1873–1876. Report on the Scientific Results of the Voyage of H.M.S.Challenger during the years 1872–76, Series Zoology, 12, 1–554.
Nygren, A., Parapar, J., Pons, J., Meißner, K., Bakken, T., Kongsrud, J.A., Oug, E., Gaeva, D., Sikorski, A., Johansen, R.A., Hutchings, P., Lavesque, N. & Capa, M. (2018) A mega-cryptic species complex hidden among one of the most common annelids in the North East Atlantic. PLoS ONE, 13 (6), e0198356.
https://doi.org/10.1371/journal.pone.0198356
O’Reilly, M. (1995) Parasitic and commensal Copepoda. In: Mackie, A.S.Y., Oliver, P.G. & Rees, E.I.S. (Eds.), Benthic biodiversity in the southern Irish Sea. Studies in Marine Biodiversity and Systematics from the National Museum of Wales. BIOMAR Reports, 1, 62–69.
O’Reilly, M. (1999) Notes on copepod parasites of polychaete worms in Scottish waters: Including the first UK records of the Californian copepod Spiophanicola spinosus Ho, 1984 (Poecilostomatoida: Spiophanicolidae). Glasgow Naturalist, 23 (4), 46–47, pl. 3.
O’Reilly, M. (2000) Notes on copepod parasites of phyllodocid polychaete worms in Scottish waters; including the first UK records of the Mediterranean copepod Phyllodicola petiti (Delamare Deboutteville & Laubier, 1960). Glasgow Naturalist, 23, 39–44.
O’Reilly, M. (2016) Parasitic and commensal polychaetes (Fams. Arabellidae and Sphaerodoridae) and copepods (Fam. Saccopsidae) associated with lamella-worms (Terebellides spp.) in Scottish, and nearby, waters. Glasgow Naturalist, 26, 61–70.
O’ Reilly, M.G. & Geddes, D. (2000) Copepoda. In: Foster-Smith, J. (Ed.), The Marine Fauna and Flora of the Cullercoats District: Marine Species Records for the North East Coast of England. Vol.1. A Dove Marine Laboratory Publication, Penshaw Press, Sunderland, pp. 217–281.
O’Reilly, M., Nowacki, S. & Bell, A. (2011) New records of scaleworms and their allies (Polychaeta: Aphroditoidea and Pisionoidea), from the Clyde and Argyll Sea Area, with notes on parasitic copepods, commensal entoprocts and other epizoans. Glasgow Naturalist, 25 (3), 49–60.
Parapar, J., Moreira, J. & Helgason, G.V. (2011) Taxonomy and distribution of Terebellides (Polychaeta, Trichobranchidae) in Icelandic waters, with the description of a new species. Zootaxa, 2983, 1–20.
Parapar, J., Moreira, J. & O'Reilly, M. (2016) A new species of Terebellides (Polychaeta: Trichobranchidae) from Scottish waters with an insight into branchial morphology. Marine Biodiversity, 46 (1), 211–225.
https://doi.org/10.1007/s12526-015-0353-5
Ruppert, E.E., Fox, R.S. & Barnes, R.D. (2004) Invertebrate Zoology. A functional evolutionary approach. Brooks/Cole, Thomson Learning, Belmont, 963pp.
Sars, M. (1870) Bidrag til Kundskab om Christianiafjordens Fauna. II. Nyt Magazin for Naturvidenskaberne, 17, 13–226, pls. 8–13.
Steenstrup, J.J.S. & Lütken, C.F. (1861) Bidrag til Kundskab om det aabne Havs Snyltekrebs og Lernaeer samt om nogle andre nye eller hidtil kun ufuldstaendigt kjendte parasitiske Copepoder. Kongelige Danske Videnskabernes Selskabs Skrifter, 5, 341–432, pls. 1–15.
https://doi.org/10.5962/bhl.title.59539
Stock, J.H. (1986) Cases of hyperassociation in the Copepoda (Herpyllobiidae and Nereicolidae). Systematic Parasitology, 8, 71–81.
https://doi.org/10.1007/BF00010311
Stock, J.H. (1996) Two new species of Copepoda parasitic on polynoid polychaetes. Crustaceana, 69, 438–445.
https://doi.org/10.1163/156854096X01023
Vanhöffen, E. (1913) Herpyllobius antarcticus n. sp. ein an Enipo rhombigera Ehlers schmarotzender Copepode. Deutsch Südpolar-Expedition, 13, 599–602.
Walter, T.C. & Boxshall, G.A. (2018) World of Copepods database. World Register of Marine Species. Available from: http://www.marinespecies.org/aphia.php?p=taxdetails&id=128574 (accessed 26 February 2019)
Wilson, C.B. (1924) New North American parasitic copepods, new hosts and notes on copepod nomenclature. Proceedings of the United States National Museum, 64 (2507), 1–22.
https://doi.org/10.5479/si.00963801.64-2507.1
WoRMS Editorial Board (2018) World Register of Marine Species. VLIZ. Available from: http://www.marinespecies.org (accessed 21 January 2018)