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Type: Article
Published: 2021-08-06
Page range: 333-364
Abstract views: 580
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The “Cribrilina annulata" problem and new species of Juxtacribrilina (Bryozoa: Cheilostomata: Cribrilinidae) from the North Pacific

Department of Biological Sciences, Faculty of Science, Hokkaido University, N10 W8, Kita-ku, Sapporo 060-0810, Japan.
Department of Invertebrate Zoology and Aquatic Ecology, Biological Faculty, Perm State National Research University, Bukirev Street 15, GSP, Perm 614990, Russia. 3A.V. Zhirmunsky National Scientific Center of Marine Biology, Far East Branch, Russian Academy of Sciences, Palchevskogo Street 17, Vladivostok 690041, Russia.
National Institute of Water and Atmospheric Research, Private Bag 14901 Kilbirnie, Wellington 6022, New Zealand.
Department of Invertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Universitetskaja nab. 7/9, Saint Petersburg 199034, Russia. Department of Palaeontology, Faculty of Earth Sciences, Geography and Astronomy, University of Vienna, Althanstr. 14, Vienna 1090, Austria.
Bryozoa Alaska Commander Islands cribrimorph evolution Japan Kamchatka Kuril Islands new species ooecium Sea of Okhotsk

Abstract

Originally described from Greenland, Juxtacribrilina annulata (Fabricius, 1780) (previously known as Cribrilina annulata) has long been regarded as having a circumpolar, Arctic-boreal distribution. The genus Juxtacribrilina Yang, Seo, Min, Grischenko & Gordon, 2018 accommodated J. annulata and three related North Pacific species formerly in Cribrilina Gray, 1848 that lack avicularia, have a reduced (hood-like, cap-like, or vestigial) ooecium closely associated with modified latero-oral spines to form an ooecial complex, and produce frontally or marginally positioned dwarf ovicellate zooids. While the recently described NW Pacific species J. mutabilis and J. flavomaris, which have a vestigial ooecium like a short, flattened spine, clearly differ from J. annulata, the differences between J. annulata and other Pacific populations remained unclear. Here we provide descriptions for five species from the North Pacific region. We identified a specimen from the Sea of Okhotsk as J. annulata. Among the other four species, J. ezoensis n. sp. has a trans-Pacific distribution (abundant at Akkeshi, Hokkaido, Japan; also detected in the Commander Islands and at Ketchikan, Southeast Alaska); J. pushkini n. sp. was found only at Ketchikan; J. dobrovolskii n. sp. was found only at Shikotan Island in the Lesser Kuril Chain; and J. tumida n. sp. was found only at Kodiak, Gulf of Alaska. These four species all differ from J. annulata in having one or two frontal pore chambers on the proximal gymnocyst of most zooids; in budding frontal dwarf ovicellate zooids from these chambers rather than from basal pore chambers; in producing dwarf zooids more abundantly; and in having ooecia that are somewhat to markedly more reduced (cap-like rather than hood-like) and more closely integrated with the modified latero-oral spines. Furthermore, in the Pacific species, the ooecium in basal zooids arises from the roof of the distal pore chamber of the maternal zooid; ovicellate zooids can thus also bud a distal autozooid and are often arranged in columnar series with other zooids. In J. annulata, the hood-like kenozooidal ooecium budded from the maternal zooid replaces the distal autozooid, and ovicellate zooids are thus usually not embedded in a columnar series.

 

References

  1. Bishop, J.D.D. (1994) The genera Cribrilina and Collarina (Bryozoa, Cheilostomatida) in the British Isles and North Sea Basin, Pliocene to present day. Zoologica Scripta, 23 (3), 225–249. https://doi.org/10.1111/j.1463-6409.1994.tb00387.x
    Bishop, J.D.D. & Househam, B.C. (1987) Puellina (Bryozoa; Cheilostomatida; Cribrilinidae) from British and adjacent waters. Bulletin of the British Museum (Natural History), Zoology, 53, 1–63.
    Busk, G. (1852) An account of the Polyzoa, and sertularian zoophytes, collected in the voyage of the Rattlesnake, on the coasts of Australia and the Louisiade Archipelago, &c. In: MacGillivray, J. (Ed.), Narrative of the Voyage of H.M.S. Rattlesnake, Commanded by the Late Captain Owen Stanley…1846–1850; Including Discoveries and Surveys in New Guinea, the Louisiade Archipelago, etc., to Which is Added the Account of Mr E. B. Kennedy’s Expedition for the Exploration of the Cape York Peninsula [Including Mr W. Carron’s Narrative]. Vol. 1. T. & W. Boone, London, pp. 343–402, pl. 1.
    Dick, M.H. & Grischenko, A.V. (2017) Rocky-intertidal cheilostome bryozoans from the vicinity of the Sesoko Biological Station, west-central Okinawa, Japan. Journal of Natural History, 51 (3–4), 141–266. https://doi.org/10.1080/00222933.2016.1253797
    Dick, M.H., Grischenko, A.V. & Mawatari, S.F. (2005) Intertidal Bryozoa (Cheilostomata) of Ketchikan, Alaska. Journal of Natural History, 39 (43), 3687–3784. https://doi.org/10.1080/00222930500415195
    Dick, M.H., Lidgard, S., Gordon, D.P. & Mawatari, S.F. (2009) The origin of ascophoran bryozoans was historically contingent but likely. Proceedings of the Royal Society B, 276, 3141–3148. https://doi.org/10.1098/rspb.2009.0704
    Dick, M.H., Mawatari, S.F., Sanner, J. & Grischenko, A.V. (2011) Cribrimorph and other Cauloramphus species (Bryozoa: Cheilostomata) from the northwestern Pacific. Zoological Science, 28 (2), 134–147. https://doi.org/10.2108/ZSJ.28.134
    Dick, M.H. & Ross, J.R.P. (1988) Intertidal Bryozoa (Cheilostomata) of the Kodiak Vicinity, Alaska. Center for Pacific Northwest Studies Occasional Paper 23. Western Washington University, Bellingham, 133 pp.
    Dick, M.H., Waeschenbach, A., Trott, T.J., Onishi, T., Beveridge, C., Bishop, J.D.D., Ito, M. & Ostrovsky, A.N. (2020) Global distribution and variation of the invasive cheilostome bryozoan Cribrilina mutabilis. Zoological Science, 37 (3), 217–231. https://doi.org/10.2108/zs190142
    Fabricius, O. (1780) Fauna Groenlandica. Ioannis Gottlob Rothe, Hafniae, 452 pp.
    Gray, J.E. (1848) List of the Specimens of British Animals in the Collection of the British Museum. Part 1. Centroniae or Radiated Animals. Trustees of the British Museum (Natural History), London, 173 pp.
    Grischenko, A.V. (1997) Bryozoans (Ctenostomida, Cheilostomida) of the Commander Islands shelf zone. In: Rzhavsky, A.V. (Ed.), Benthic flora and fauna of the shelf zone of the Commander Islands. Dal’nauka, Vladivostok, pp. 153–192. [in Russian with English summary]
    Grischenko, A.V. (2004) Intertidal Bryozoa of the Commander Islands. In: Tokranov, A.M. (Ed.) Conservation of biodiversity of Kamchatka and coastal waters. Materials of 5th scientific conference. KamchatNIRO Press, Petropavlovsk-Kamchatsky, pp. 38–43. (In Russian).
    Grischenko, A.V., Dick, M.H. & Mawatari, S.F. (2007) Diversity and taxonomy of intertidal Bryozoa (Cheilostomata) at Akkeshi Bay, Hokkaido, Japan. Journal of Natural History, 41 (17–20), 1047–1161. https://doi.org/10.1080/00222930701391773
    Grischenko, A.V., Gordon, D.P. & Melnik, V.P. (2018) Bryozoa (Cyclostomata and Ctenostomata) from polymetallic nodules in the Russian exploration area, Clarion–Clipperton Fracture Zone, eastern Pacific Ocean—taxon novelty and implications of mining. Zootaxa, 4484 (1), 1–91. https://doi.org/10.11646/zootaxa.4484.1.1
    Hassall, A.H. (1841) Supplement to a catalogue of Irish zoophytes. Annals and Magazine of Natural History, Series 1, 7 (45), 363–373. https://doi.org/10.1080/03745484109442710
    Hayward, P.J. & Ryland, J.S. (1998) Cheilostomatous Bryozoa, Part 1, Aeteoidea—Cribrilinoidea. Synopses of the British Fauna, New Series, 10, 1–366. [2nd Edition]
    Hincks, T. (1879) On the classification of the British Polyzoa. Annals and Magazine of Natural History, Series 5, 3 (14), 153–164. https://doi.org/10.1080/00222937908682494
    Ito, M., Onishi, T. & Dick, M.H. (2015) Cribrilina mutabilis n. sp., an eelgrass-associated bryozoan (Gymnolaemata: Cheilostomata) with large variation in zooid morphology related to life history. Zoological Science, 32 (5), 485–497. https://doi.org/10.2108/zs150079
    Jullien, J. (1886) Les Costulidées, nouvelle famille de Bryozoaires. Bulletin de la Société zoologique de France, 11, 601–620.
    Kluge, G.A. (1975) Bryozoa of the Northern Seas of the USSR. Amerind Publishing, New Delhi, 711 pp. [English translation of 1962 Russian volume]
    Levinsen, G.M.R. (1909) Morphological and Systematic Studies on the Cheilostomatous Bryozoa. Nationale Forfatterers Forlag, Copenhagen, 364 pp. https://doi.org/10.5962/bhl.title.5690
    Lidgard, S., Carter, M.C., Dick, M.H., Gordon, D.P. & Ostrovsky, A.N. (2012) Division of labor and recurrent evolution of polymorphisms in a group of colonial animals. Evolutionary Ecology, 26 (2), 233–257. https://doi.org/10.1007/s10682-011-9513-7
    López-Gappa, J., Pérez, L.M., Almeida, A.C.S., Iturra, D., Gordon, D.P. & Viera, L.M. (2021) Three new cribrimorph bryozoans (order Cheilostomatida) from the early Miocene of Argentina, with a discussion on spinocystal shield morphologies. Journal of Paleontology, 95 (3), 568–582. https://doi.org/10.1017/jpa.2020.108
    Martha, S.O., Vieira, L.M., Souto-Derungs, J., Grischenko, A.V., Gordon, D.P. & Ostrovsky, A.N. (2020) 11. Gymnolaemata, Cheilostomata. In: Schwaha, T. (Ed.), Phylum Bryozoa. De Gruyter, Berlin, pp. 317–423. https://doi.org/10.1515/9783110586312-011
    Nekliudova, U.A., Shunkina, K.V., Grishankov, A.V., Varfolomeeva, M.N., Granovitch, A.I. & Ostrovsky, A.N. (2019) Colonies as dynamic systems: reconstructing the life history of Cribrilina annulata (Bryozoa) on two algal substrates. Journal of the Marine Biological Association of the United Kingdom, 99 (6), 1363–1377. https://doi.org/10.1017/S0025315419000286
    Nikulina, E.A. (2002) The evolution of colony morphogenesis in bryozoans of the order Cheilostomata. Paleontological Journal, 36 (Supplement 4), 5353–5428.
    Norman, A. (1903) Notes on the natural history of East Finmark, Polyzoa. Annals and Magazine of Natural History, Series 7, 12, 81–128. https://doi.org/10.1080/00222930308678831
    O’Donoghue, C.H. & O’Donoghue, E. (1923) A preliminary list of Polyzoa (Bryozoa) from the Vancouver Island region. Contributions to Canadian Biology, New Series, 1, 1–59, pls. 1–4.
    O’Donoghue, C.H. & O’Donoghue, E. (1926) A second list of Bryozoa (Polyzoa) from the Vancouver Island region. Contributions to Canadian Biology and Fisheries, New Series, 3, 1–85, pls. 1–5.
    Osburn, R.C. (1912) The Bryozoa of the Woods Hole region. Bulletin of the Bureau of Fisheries, 30, 205–266. https://doi.org/10.5962/bhl.title.1325
    Osburn, R.C. (1950) Bryozoa of the Pacific coast of America. Part 1. Cheilostomata-Anasca. Report of the Allan Hancock Pacific Expeditions, 14, 1–269. https://doi.org/10.5962/bhl.title.6542
    Ostrovsky, A.N. (1998) Comparative studies of ovicell anatomy and reproductive patterns in Cribrilina annulata and Celleporella hyalina (Bryozoa: Cheilostomatida). Acta Zoologica, 79 (4), 287–318. https://doi.org/10.1111/j.1463-6395.1998.tb01280.x
    Ostrovsky, A.N. (2002) Brood chambers in cribrimorphs evolved by fusion of costae: further arguments. In: Wyse Jackson, P.N., Buttler, C.J. & Spencer Jones, M. (Eds.), Bryozoan studies 2001. A.A. Balkema Publishers, Lisse, pp. 247–255.
    Ostrovsky, A.N. (2008) Brood chambers in cheilostome Bryozoa: diversity and revised terminology. In: Hageman, S.J., Key, M.M.J. Jr. & Winston, J.E. (Eds.), Proceedings of the 14th International Bryozoology Association Conference, Boone, North Carolina, 1–8 July 2007. Special Publication No. 15. Virginia Museum of Natural History, Martinsville, Virginia, pp. 195–204.
    Ostrovsky, A.N. (2013) Evolution of Sexual Reproduction in Marine Invertebrates. Example of Gymnolaemate Bryozoans. Springer, Dordrecht, 356 pp. https://doi.org/10.1007/978-94-007-7146-8
    Ostrovsky, A.N. (2020) Sexual reproduction in Bryozoa. In: Schwaha, T.F. (Ed.), Handbook of Zoology. Phylum Bryozoa. De Gruyter, Berlin, pp. 101–121. https://doi.org/10.1515/9783110586312-004
    Ostrovsky, A.N., Dick, M.H. & Mawatari, S.F. (2007) The internal-brooding apparatus in the bryozoan genus Cauloramphus (Cheilostomata: Calloporidae) and its inferred homology to ovicells. Zoological Science, 24 (12), 1187–1196.
    https://doi.org/10.2108/zsj.24.1187
    Ostrovsky, A.N., Grischenko, A.V., Taylor, P.D., Bock, P. & Mawatari, S.F. (2006) Comparative anatomical study of internal brooding in three anascan bryozoans (Cheilostomata) and its taxonomic and evolutionary implications. Journal of morphology, 267 (6), 739–749. https://doi.org/10.1002/jmor.10438
    Ostrovsky, A.N., Nielsen, C., Vávra, N. & Yagunova, E.B. (2009a) Diversity of brood chambers in calloporid bryozoans (Gymnolaemata, Cheilostomata): comparative anatomy and evolutionary trends. Zoomorphology, 128, 13–35. https://doi.org/10.1007/s00435-008-0070-8
    Ostrovsky, A.N., O'Dea, A. & Rodríguez, F. (2009b) Comparative anatomy of internal incubational sacs in cupuladriid bryozoans and the evolution of brooding in free-living cheilostomes. Journal of Morphology, 270, 1413–1430. https://doi.org/10.1002/jmor.10767
    Powell, N.A. (1967) Sexual dwarfism in Cribrilina annulata (Cribrilinidae–Bryozoa). Journal of the Fisheries Research Board of Canada, 24 (9), 1905–1910. https://doi.org/10.1139/f67-157
    Powell, N.A. (1968) Bryozoa (Polyzoa) of Arctic Canada. Journal of the Fisheries Research Board of Canada, 25 (11), 2269–2320. https://doi.org/10.1139/f68-202
    Silén, L. (1942) Origin and development of the cheilo-ctenostomatous stem of Bryozoa. Zoologiska Bidrag Fran Uppsala, 22, 1–59.
    Smitt, F.A. (1868) Bryozoa marina in regionibus arcticis et borealibus viventia recensuit. Öfversigt af Kongliga Vetenskaps-Akademiens Förhandlingar, 24, 443–487.
    Yagunova, E.B. & Ostrovsky, A.N. (2008) Encrusting colonies of Bryozoa: life in two dimensions. JMBA Global Marine Environment, 8, 1–3.
    Yagunova, E.B. & Ostrovsky, A.N. (2010) The influence of substrate type on sexual reproduction of the bryozoan Cribrilina annulata (Gymnolaemata, Cheilostomata): a case study from Arctic seas. Marine Biology Research, 6 (3), 263–270. https://doi.org/10.1080/17451000903147443
    Yang, H.J., Seo, J.E, Min, B.S., Grischenko, A.V. & Gordon, D.P. (2018) Cribrilinidae (Bryozoa: Cheilostomata) of Korea. Zootaxa, 4377 (2), 216–234. https://doi.org/10.11646/zootaxa.4377.2.4

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