Abstract
The genera Lagenophrys Stein, 1852, Paralagenophrys Clamp, 1987, Clistolagenophrys Clamp, 1991, and Operculigera Kane, 1969 make up the family Lagenophryidae and, together, contain more than 80 species worldwide that live mainly as ectosymbionts of crustaceans. Lagenophryids are characterized by possession of a lorica, but the lorica aperture and the associated parts of the body differ between genera. Despite their widespread distribution, relatively few papers have been published on lagenophryids in recent years, and the present paper is intended to promote research on lagenophryids by providing an annotated checklist of all known species and a brief review of the family, including data of their geographic distribution and their hosts.
References
Abonyi, A. (1928) Über die epizoen der Orchestia cavimana (Heller). Arbeiten des Ungarischen Biologischen Forschungs-Institutes, 2, 5–23.
Aladro-Lubel, M.A. & Sánchez-Calderón, M.G. (2005) Ciliados epibiontes de la vegetación sumergida y de los invertebrados de la laguna de Tecocomulco. In: Huizar, A.R., Jiménez, F.E. & Juárez, C. (Eds.), La laguna de Tecocomulco. Geo-ecología de un desastre. Publicación Especial 3. Instituto de Geología, Universidad Nacional Autónoma de México. México, pp. 169–178.
Aladro-Lubel, M.A., Mayén-Estrada, R. & Reyes-Santos, M. (2006) Registro actualizado de ciliados (Agosto, 2004). Listados faunísticos de México. XI. Instituto de Biología Universidad Nacional Autónoma de México, México, 97 pp.
Becker, G. (1968) On the biology, physiology and ecology of marine wood-boring crustaceans. In: Gareth-Jones, E.B. & Eltringham, S.K. (Eds.), Marine Borers, Fungi, and Fouling Organisms of wood. Organisation for Economic Co-operation and Development, Paris, pp. 303–326.
Boshko, E.G. (1992) Commensal loricate peritrichs on crustaceans of the Dnieper Basin. Tsitologiya, 34, 32.
Boshko, E.G. (1995) New species of Infusoria of the genera Sincothurnia and Lagenophrys (Peritricha, Vaginicolidae, Lagenophryidae). Zoologicheskii Zhurnal, 74, 5–9.
Boshko, E.G. (1996) New species of commensal peritrichs from the genera Sincothurnia and Lagenophrys (Peritricha, Vaginicolidae, Lagenophryidae). Hydrobiological Journal, 32,101–106.
Bütschli, O. (1887–1889) Protozoa. Abt. III. Infusoria und System der Radiolaria. In: Bronn, H.G. (Ed.), Klassen und Ordnung des Thiers-Reichs, Vol. I. C. F. Winter, Leipzig, Germany, pp. 1098–2035.
Clamp, J.C. (1973) Observations on the host-symbiont relationships of Lagenophrys lunatus Imamura. Journal of Protozoology, 20, 558–561.
http://dx.doi.org/10.1111/j.1550-7408.1973.tb03572.xClamp, J.C. (1984) A revision of the family Lagenophryidae Bûtschli, 1889, and description of the family Pseudolagenophryidae n. fam. [Ph.D. Thesis]. [North Carolina, USA]: North Carolina State University.
Clamp, J.C. (1987a) Five new species of Lagenophrys (Ciliophora, Peritricha, Lagenophryidae) from the United States with observations on their developmental stages. Journal of Protozoology, 34, 382–392.
http://dx.doi.org/10.1111/j.1550-7408.1987.tb03197.x
Clamp, J.C. (1987b) Redescription of Paralagenophrys singularis (Kellicott) n. comb. (Ciliophora: Peritrichia: Lagenophryidae). Journal of Protozoology, 34, 249–253.
http://dx.doi.org/10.1111/j.1550-7408.1987.tb03168.xClamp, J.C. (1988a) A new species of Lagenophrys (Ciliophora: Peritricha: Lagenophryidae) ectocommensal on the wood-boring isopod Limnoria (Flabellifera: Limnoridae). Transactions of the American Microscopical Society, 107, 12–16.
http://dx.doi.org/10.2307/3226400
Clamp, J.C. (1988b) The occurrence of Lagenophrys aselli (Ciliophora, Peritricha, Lagenophryidae) in North America and a description of environmentally induced morphological variation in the species. Transactions of the American Microscopical Society, 107, 17–27.
http://dx.doi.org/10.2307/3226402
Clamp, J.C. (1988c) Lagenophrys anticthos N. sp. and L. aegleae Mouchet-Bennati, 1932 (Ciliophora, Peritricha, Lagenophryidae), ectocommensals of South American crustaceans. Journal of Protozoology, 35, 164–169. http://dx.doi.org/10.1111/j.1550-7408.1988.tb04097.x
Clamp, J.C. (1989) Redescription of Lagenophrys eupagurus Kellicott (Ciliophora, Peritricha, Lagenophryidae) and a comparison of it with three similar species. Journal of Protozoology, 36, 596–607.
http://dx.doi.org/10.1111/j.1550-7408.1989.tb01102.x
Clamp, J.C. (1990a) Redescription of three species of Lagenophrys (Ciliophora, Peritricha, Lagenophryidae) and a new North American species of Lagenophrys from hypogean amphipods. Transactions of the American Microscopical Society, 109, 1–31.
http://dx.doi.org/10.2307/3226589Clamp, J.C. (1990b) A new species of Lagenophrys (Ciliophora, Peritricha, Lagenophryidae) ectocommensal on North American species of Gammarus (Crustacea: Amphipoda). Transactions of the American Microscopical Society, 109, 121–128.
http://dx.doi.org/10.2307/3226806
Clamp, J.C. (1991) Revision of the family Lagenophryidae Bütschli, 1889 and description of the family Usconophryidae n. fam. (Ciliophora, Peritricha). Journal of Protozoology, 38, 355–377.
http://dx.doi.org/10.1111/j.1550-7408.1991.tb01373.x
Clamp, J.C. (1992) Three new species of lagenophryid peritrichs (Ciliophora) ectocommensal on freshwater decapod crustaceans from Madagascar. Journal of Protozoology, 39, 732–740.
http://dx.doi.org/10.1111/j.1550-7408.1992.tb04456.x
Clamp, J.C. (1993) A new species of Lagenophrys (Ciliophora: Peritrichia) symbiotic on marine amphipods. Transactions of the American Microscopical Society, 112, 62–68.
http://dx.doi.org/10.2307/3226782
Clamp, J.C. (1994) New species of Lagenophrys (Ciliophora, Peritrichia) from New Zealand and Australia. Journal of Eukaryotic Microbiology, 41, 343–349.
http://dx.doi.org/10.1111/j.1550-7408.1994.tb06088.xClamp, J.C. (2005) Redescription of Lagenophrys maxillaris (Jankowski, 1993) (Ciliophora, Peritrichia, Lagenophryidae), an ectocommensal of marine amphipods. Journal of Eukaryotic Microbiology, 52, 38–43.
http://dx.doi.org/10.1111/j.1550-7408.2005.3302r.xClamp, J.C. (2006) Redescription of Lagenophrys cochinensis Santhakumari & Gopalan, 1980 (Ciliophora, Peritrichia, Lagenophryidae), an ectosymbiont of marine isopods, including new information on morphology, geographic distribution, and intraspecific variation. Journal of Eukaryotic Microbiology, 53, 58–64.
http://dx.doi.org/10.1111/j.1550-7408.2005.00074.x
Clamp, J.C. & Kane J.R. (2003) Redescription of four species of lagenophryid peritrichs (Ciliophora) from Australia and New Guinea, with descriptions of two new species. Records of the Australian Museum, 55, 153–168.
http://dx.doi.org/10.3853/j.0067-1975.55.2003.1381Claps, M.C. & Sampóns, M.R. (1994) First record of Lagenophrys discoidea Kellicott (Ciliophora, Peritrichia, Lagenophryidae), ectocommensal of argentinian ostracods. Iheringia Série Zoologia, 76, 167–170.
Corliss, J.O. & Brough, I.M. (1965) A new species of Lagenophrys (Ciliata: Peritrichida) from the Jamaican crab Metopaulias depressus. Transactions of the American Microscopical Society, 84, 73–80.
http://dx.doi.org/10.2307/3224542
Couch, J. A. (1966) Two peritrichous ciliates from the gills of the blue crab. Chesapeake Science, 7, 171–173.
http://dx.doi.org/10.2307/1351165
http://dx.doi.org/10.1007/BF02854045Couch, J.A. (1967) A new species of Lagenophrys (Ciliatea: Peritrichida: Lagenophryidae) from a marine crab, Callinectes sapidus. Transactions of the American Microscopical Society, 86, 204–211.
http://dx.doi.org/10.2307/3224692
Couch, J.A. (1973) Ultrastructural and protargol studies of Lagenophrys callinectes (Ciliophora: Peritrichida). Journal of Protozoology, 2, 638–647.
http://dx.doi.org/10.1111/j.1550-7408.1973.tb03588.xCouch, J.A. (1978) Diseases, parasites, and toxic responses of commercial penaeid shrimps of the Gulf of Mexico and South Atlantic coasts of North America. Fishery Bulletin, 76, 1–44.
Debaisieux, P. (1959) Lagenophrys lunatus, Ima (Ciliate, Péritriche). Cellule, 59, 359–383.
Felgenhauer, B.E. (1979) A note on the scanning electron microscopy and hosts of the widespread peritrich ciliate Lagenophrys labiata. Transactions of the American Microscopical Society, 98, 591–595.
http://dx.doi.org/10.2307/3225916
Felgenhauer, B.E. (1982) A new species of Lagenophrys (Ciliophora: Peritrichida) from the freshwater shrimp Palaemonetes kadiakensis. Transactions of the American Microscopical Society, 101, 142–150.
http://dx.doi.org/10.2307/3225767Felgenhauer, B.E. & Ridgeway, B.T. (1977) A note on the occurrence of the peritrich ciliate Lagenophrys sp. on the freshwater shrimp Palaemonetes kadiakensis in Illinois. Transactions of the American Microscopical Society, 96, 533–535.
http://dx.doi.org/10.2307/3225673Fenchel, T. (1965) On the ciliate fauna associated with the marine species of the amphipod genus Gammarus J. G. Fabricius. Ophelia, 2, 281–303.
http://dx.doi.org/10.1080/00785326.1965.10409605Fernandez-Leborans, G. (2009) A review of recently described epibioses of ciliate Protozoa on Crustacea. Crustaceana, 82, 167-189.
Fernandez-Leborans, G. & Tato-Porto, M.L. (2000) A review of the species of protozoan epibionts of crustaceans. Crustaceana, 73, 643–683. Avaliable from: http://www.jstor.org/stable/20106331 (Accessed 17 Jun. 2016)
Finley, H.E. (1943) The conjugation of Vorticella microstoma. Transactions of the American Microscopical Society, 62, 97–121.
http://dx.doi.org/10.2307/3222915
Finley, H.E. (1946) Patterns of sexual reproductive cycles in ciliates. Biodynamica, 6, 31–79.
Green, J. (1974) Parasites and epibionts of Cladocera. Transactions of the Zoological Society of London, 32, 418–514.
http://dx.doi.org/10.1111/j.1096-3642.1974.tb00031.x
Imamura, T. (1940) Two species of Lagenophrys from Sapporo. Annotationes Zoologicae Japonenses 19(4), 267–270.
Jakschik, H. (1967a) A comparative study of the ciliate fauna of subterranean and epigean amphipods of central Illinois. Journal of Protozoology, 14 (Suppl.), 24.
Jakschik, H. (1967b) Distribution of the ciliate fauna associated with the subterranean fresh-water amphipod, Bactrurus mucronatus (Forbes) Hay. Master´s Thesis, University of Illinois.
Jankowski, A.W. (1986) New and little known genera of ciliated protozoa (Phylum Ciliophora). In: Krylov, M.V. (Ed.), Systematics of Protozoa and their phylogenetic links with lower Eukaryotes. Trudy Zoologicheskogo Instituta Akademii Nauk SSSR 144, pp. 72–88.
Jankowski, A.W. (1993) Taxonomy of Ciliophora. 2. New species of Opercularia, Entziella and Circolagenophrys from the Black Sea and Pacific, and taxonomic notes on other peritrichs (Peritricha). Zoosystematica Rossica, 2, 217–222.
Ji, D., Song, W. & Warren, A. (2006) Redescriptions of three marine peritrichous ciliates, Zoothamnium alternans Claparède et Lachmann, 1859, Z. sinense Song, 1991 and Z. commune Kahl, 1933 (Ciliophora, Peritrichia), from North China. Acta Protozoologica, 45, 27-39.
Johnson, S.K. (1974) Ectocommensals and parasites of shrimp from Texas rearing ponds. Texas A&M University Sea Grant Program Publications, TAMU-SG-74-207, 1–19.
Johnson, S.K. (1975) Handbook of shrimp diseases. Texas A&M University Sea Grant Program Publications, TAMU-SG-75-603, 4–23.
Kahl, A. (1935) Urtiere oder Protozoa. I. Wimpertiere oder Ciliata (Infusoria), 4. Peritricha und Chonotricha. In: Dahl, F. (Ed.), Die Tierwelt Deutschlands (Part 30), G. Fischer, Jena, pp. 651–805.
Kane, J.R. (1965) The genus Lagenophrys Stein, 1852 (Ciliata, Peritricha) on Australasian Parastacidae. Journal of Protozoology, 12, 109–122.
http://dx.doi.org/10.1111/j.1550-7408.1965.tb01823.xKane, J.R. (1969) The Lagenophryidae in Australia and South Africa. In: Strelkov, A. A., Sukhanova, K.M. & Raĭkov, I.B. (Eds.), Progress in Protozoology; abstracts of papers read at the IIIrd International Congress on Protozoology, Leningrad, 2-10 July, 1969. Leningrad, Nauka, pp. 368–369.
Keiser, A. (1921) Die sessilen peritrichen Infusorien und Suctorien von Basel und Umgebung. Revue Suisse de Zoologie, 28, 221–341.
Kellicott, D.S. (1885) Observations on infusoria, with descriptions of new species. Proceedings of the American Society of Microscopists, 7, 110–124.
http://dx.doi.org/10.2307/3220579Kellicott, D.S. (1887) Some new and rare infusoria. Proceedings of the American Society of Microscopists, 9, 187–190.
http://dx.doi.org/10.2307/3220551
Kellicott, D.S. (1893) On certain marine infusoria observed at Woods Hole, Mass. Annual Report of the Ohio Academy of Science, 2, 10–11.
Lust, S. (1950) Zwei auf Ostracoden lebende Lagenophrys-Arten (Ciliata, Peritricha). Zoologische Jahrbücher. Abteilung für Systematik Ökologie und Geographie der Tiere, 79, 350–352.
Mayén-Estrada R. & Aladro-Lubel, M.A. (2000) First record of Lagenophrys dennisi (Ciliophora: Peritrichia) on the exoskeleton of crayfish Cambarellus patzcuarensis. Journal of Eukaryotic Microbiology, 47, 57–61.
http://dx.doi.org/10.1111/j.1550-7408.2000.tb00011.xMayén-Estrada, R. & Aladro-Lubel, M.A. (2006) Lagenophrys lenticula and L. patina (Peritricha), epibionts of Hyalella azteca (Amphipoda). A study using scanning electron microscopy to reveal details of the lorica aperture. Protistology, 4, 339–345.
Mayén-Estrada, R. & Aguilar-Aguilar, R. (2012) Track analysis and geographic distribution of some Lagenophrys Stein, 1852 (Protozoa: Ciliophora: Peritrichia) species. Journal of Natural History, 46, 249–263.
http://dx.doi.org/10.1080/00222933.2011.626531Messick, G.A. (1998) Diseases, parasites, and symbionts of blue crabs (Callinectes sapidus) dredged from Chesapeake Bay. Journal of Crustacean Biology, 18, 533–548.
http://dx.doi.org/10.1163/193724098X00368Mohr, J.L. (1959) On the protozoan associates of Limnoria. In: Ray, D.L. (Ed.), Marine Boring and Fouling Organisms. University of Washington Press, Seattle, pp. 84–91.
Monard, A. (1920) La faune profonde du Lac de Neuchatel. Bulletin de la Société Neuchâteloise des Sciences Naturelles, 44, 65–235.
Mouchet-Bennati, S. (1932) Sur la branchie d’ Aeglea laevis (Latreille) et son parasite Lagenophrys aeglea nov. sp. Comptes Rendus des Seances de la Societe de Biologie et de ses Filiales, 109, 148–150.
Nie, D. & Ho, Y.L. (1943) Notes on some epizoic infusoria from the freshwater shrimp, Palaemon nipponensis. Sinensia, 14, 143–149.
Penard, E. (1922) Etudes sur les Infusoires d’Eau Douce. Georg et Cie, Geneva, 331 pp.
http://dx.doi.org/10.5962/bhl.title.11630Piezik, Z. (1975) Epizoic ciliates occurring on gammarids of the subgenus Rivulogammarus Karaman from streams in the vicinity of Poznan. Badania Fizjograficzne nad Polską Zachodnią. Seria C, Zoologia, 28, 41–77.
Piezik, Z. (1976) Epizoic ciliata on Asellus aquaticus (L.) in stagnant waters of Szczecin. Badania Fizjograficzne nad Polska Zachodnia, 29, 139–150.
Plate, L. (1889) Studien über Protozoan. Zoologische Jahrbücher, Abteilung für Anatomie und Ontogenie der Tiere, 3, 135–198.
Roberts, G.N. & Chubb, J.C. (1998) The distribution and locations of the symbiont Lagenophrys aselli on the freshwater isopod Asellus aquaticus. Freshwater Biology, 40, 671–677.
http://dx.doi.org/10.1046/j.1365-2427.1998.00365.xRustige, K.H. (1991) Eine Bestmmungshile für die epizoischen Ciliaten der einheimischen Gammariden. Bericht Naturwissenschaftlicher Verein für Bielefeld und Umgegend, 32, 263–290.
Rustige, K.H. & Mannesmann, R. (1991) Die Verbreitung der epizoischen ciliaten von Gammarus pulex L. im Johannisbachsystem des Ravensberger Hügellandes (Ostwestfalen). Bericht Naturwissenschaftlicher Verein für Bielefeld und Umgegend, 32, 291–321.
Santhakumari, V. (1976) Seasonal incidence and relative abundance of associated organisms of the wood boring isopods Sphaeroma terebrans and S. annandalei. Journal of the Marine Biological Association of India, 18, 91–98.
Santhakumari, V. & Gopalan, U.K. (1980) The protozoan associates of some crustaceans. Mahasagar Bulletin of the National Institute of Oceanography, 13, 125–131.
Santhakumari, V. & Nair, B. (1982) Observations on the parasites and associates of wood-boring molluscs and crustaceans of the southwest coast of India. Fishery Technology, 19, 65–73.
Santhakumari, V. & Nair, B. (1985) Some ciliates from the marine wood-boring isopod Sphaeroma. Indian Journal of Fisheries, 32, 215–223.
Schödel, H. (1983) Three new Peritricha on Gammaridae. Archiv für Protistenkunde, 127, 115–126.
http://dx.doi.org/10.1016/S0003-9365(83)80010-4Shomay, D. (1954a) The structure and life history of Lagenophrys labiata Stokes (Ciliata, Peritrichia). Journal of Protozoology, (Suppl.), 1, 2.
Shomay, D. (1954b) The natural history of Lagenophrys labiata Stokes (Ciliata, Peritrichia). Journal of Protozoology, (Suppl.), 1, 9.
Sprague, V. (1970) Some protozoan parasites and hyperparasites in marine decapod crustacean. In: Snieszko, S.F. (Ed.). A Symposium on Diseases of Fishes and Shellfishes. American Fisheries Society Special Publication, 5, 416–430.
Sprague, V. & Couch, J.A. (1971) An annotated list of protozoan parasites, hyperparasites, and commensals of decapod crustaceans. Journal of Protozoology, 18, 526–537.
http://dx.doi.org/10.1111/j.1550-7408.1971.tb03367.xStammer, H.J. (1935) Zwei neue troglobionte Protozoen: Spelaeophrya troglocaridis n. g., n. sp. von den Antennen der Höhlengarnele Troglocaris schmidti Dorm. und Lagenophrys monolistrae n. sp. von den Kiemen (Pleopoden) der Höhlenasselgattung Monolistra. Archiv für Protistenkunde, 84, 518–527.
Stein, F. (1852) Neue Beitrage zur Kenntnis der Entwicklungsgeschichte und des feineren Baues der Infusionsthiere. Zeitschrift für wissenschaftliche Zoologie, 3, 475–509.
Stiller, J. (1971) Szájkoszorús csillósok- Peritricha. Fauna Hungariae (Magyarország Állatvilága), 105, 1–245.
Stokes, A.C. (1887) IV. Notices of new American fresh-water infusoria. Journal of the Royal Microscopical Society, 1887, 35–40.
http://dx.doi.org/10.1111/j.1365-2818.1887.tb01561.xStokes, A.C. (1888) A preliminary contribution toward a history of the fresh-water infusoria of the United States. Journal of the Trenton Natural History Society, 1, 71–344.
Stokes, A.C. (1890) Notices of new fresh–water infusoria. Proceedings of the American Philosophical Society, 28, 74-80.
Sun, P., Song, W., Clamp, J. & Al-Rasheid, K.A.S. (2006) Taxonomic characterization of Vorticella fusca Precht, 1935 and Vorticella parapulchella n. sp., two marine peritrichs (Ciliophora, Oligohymenophorea) from China. Journal of Eukaryotic Microbiology, 53, 348–357.
http://dx.doi.org/10.1111/j.1550-7408.2006.00112.xSwarczewsky, B. (1930) Zur Kenntnis der Baikalprotistenfauna. Die an den Baikalgammariden lebenden Infusoria. VII. Lagenophrys, Vaginicola und Cothurnia. Archiv für Protistenkunde, 69, 455–532.
Thomsen, R. (1945) Sobre Lagenophrys lenticulata (Kellicot) (Protozoa Ciliata). Comunicaciones Zoológicas del Museo de Historia Natural de Montevideo, 1, 1–9.
Trueba, F.J. (1978) A taxonomic revision of the peritrich ciliate genus Pyxicola. Beaufortia, 27, 219–243.
Trueba, F.J. (1980) A taxonomic revision of the peritrich ciliate genera Thuricola and Pseudothuricola. Beaufortia, 30, 125–138.
Vidal-Martínez, V.M., Jiménez-Cueto, A.M. & Simá-Alvarez, R. (2002) Parasites and symbionts of native and cultured shrimps from Yucatán, Mexico. Journal of Aquatic Animal Health, 14, 57–64.
http://dx.doi.org/10.1577/1548-8667(2002)014<0057:PASONA>2.0.CO;2
Von Ubisch, M. (1913) Ein Beitrag zur Kenntnis der Gattung Lagenophrys. Archiv für Protistenkunde, 29, 39–77.
Walker, M.H., Roberts, E.M. & Usher, M.L. (1986) The fine structure of the trophont and stages in telotroch formation in Circolagenophrys ampulla (Ciliophora, Peritrichida). Journal of Protozoology, 33, 246–255.
http://dx.doi.org/10.1111/j.1550-7408.1986.tb05601.xWallengren, H. (1900) Uebersicht von der Gattung Lagenophrys St. Biologisches Zentrablatt, 20, 358–363.
Wang, C.C. & Nie, D. (1933) Report on the rare and new species of freshwater infusoria, part I. Contributions from the Biological Laboratory of the Science Society of China, Zoolological Series, 10, 1–99.
Warren, A. (1986) A revision of the genus Vorticella (Ciliophora: Peritrichida). Bulletin of the British Museum (Natural History) (Zoology), 50, 1–57.
Willis, A.G. (1942) Studies on Lagenophrys tattersalli sp. n. (Ciliata, Peritricha, Vorticellinae). I. Structure, asexual reproduction and metamorphosis. Quarterly Journal of Microscopical Science, 83, 171–196.
Zhan, Z., Xu, K., Warren, A. & Gong, Y. (2009) Reconsideration of phylogenetic relationships of the Subclass Peritrichia (Ciliophora, Oligohymenophorea) based on small subunit ribosomal RNA gene sequences, with the establishment of a new subclass Mobilia Kahl, 1933. Journal of Eukaryotic Microbiology, 56, 552–558.
http://dx.doi.org/10.1111/j.1550-7408.2009.00435.x