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The life cycle of Gyliauchen volubilis Nagaty, 1956 (Digenea: Gyliauchenidae) from the Red Sea

Published online by Cambridge University Press:  05 May 2011

M.O. Al-Jahdali*
Affiliation:
Biological Sciences Department, Rabigh-Faculty of Science and Arts, King Abdulaziz University, P.O. Box 344, Rabigh21911, Saudi Arabia
R.M. El-Said Hassanine
Affiliation:
Biological Sciences Department, Rabigh-Faculty of Science and Arts, King Abdulaziz University, P.O. Box 344, Rabigh21911, Saudi Arabia

Abstract

Although nothing is known about gyliauchenid life cycles, molecular phylogenetic studies have placed the Gyliauchenidae Fukui, 1929 close to the Lepocreadiidae Odhner, 1905. The gyliauchenid Gyliauchen volubilis Nagaty, 1956 was found in the intestine of its type-host, Siganus rivulatus, a siganid fish permanently resident in a lagoon within the mangrove swamps on the Egyptian coast of the Gulf of Aqaba. Larval forms of this trematode (mother sporocysts, rediae and cercariae) were found in the gonads and digestive gland of Clypeomorus clypeomorus (Gastropoda: Cerithiidae), a common snail in the same lagoon. So, this life cycle of G. volubilis was elucidated under natural conditions: eggs are directly ingested by the snail; mother sporocysts and rediae reach their maturity 3–6 and 11–13 weeks post-infection; rediae contain 23–29 developing cercariae; fully developed cercariae are gymnocephalus, without penetration glands, emerge from the snail during the night 16–18 weeks post-infection and rapidly encyst on aquatic vegetation (no second intermediate host); encysted metacercariae are not progenetic; 4-day-old metacercariae encysted on filamentous algae fed to S. rivulatus developed into fully mature worms 6–8 weeks post-infection. The cycle was completed in about 26 weeks and followed one of the three known patterns of lepocreadiid life cycles, and except for the gymnocephalus cercariae, the other larval stages are very similar to those of lepocreadiids. Generally, the life cycle of G. volubilis implicitly supports the phylogenetic relationship of Gyliauchenidae and Lepocreadiidae inferred from molecular phylogenetic studies.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2011

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References

Barker, S.C., Blair, D., Cribb, T.H. & Tonion, K. (1993) Phylogenetic position of Heronimus mollis (Digenea): evidence from 18S ribosomal RNA. International Journal for Parasitology 23, 533536.CrossRefGoogle ScholarPubMed
Bartoli, P. & Prevot, G. (1967) Étude du cycle evolutif d'un trematode peu connu: Lepocreadium pegorchis (M. Stossisch, 1900) (Trematoda: Digenea). Annales de Parasitologie Humaine Comparée 42, 605619.CrossRefGoogle Scholar
Blair, D. & Barker, S.C. (1993) Affinities of the Gyliauchenidae: utility of the 18S rRNA gene for phylogenetic inference in the Digenea (Platyhelminthes). International Journal for Parasitology 23, 527532.CrossRefGoogle ScholarPubMed
Bozhkov, D.K. (1982) Helminths. Life cycle and their evolution. pp. 1117. Sofia, Nauka i Izkustvo.Google Scholar
Bray, R.A. (2005) Superfamily Lepocreadioidae Odhner, 1905. pp. 543678in Jones, A., Bray, R.A. & Gibson, D.I. (Eds) Keys to the Trematoda. Vol. 2. London, CABI Publishing and the Natural History Museum.Google Scholar
Bray, R.A., Waeschenbach, A., Cribb, T.H., Weedall, G.D., Dyal, P. & Littlewood, D.T.J. (2009) The phylogeny of the Lepocreadioidea (Platyhelminthes, Digenea) inferred from nuclear and mitochondrial genes: implications for their systematics and evolution. Acta Parasitologica 54, 310329.CrossRefGoogle Scholar
Brooks, D.R., O'Grady, R.T. & Glen, D.R. (1985) Phylogenetic analysis of the Digenea (Platyhelminthes: Cercomeria) with comments on their adaptive radiation. Canadian Journal of Zoology 63, 411443.CrossRefGoogle Scholar
Caballero, E. & Bravo-Hollis, M. (1953) Ichthyotrema vogelsangi n. g., n. sp. (Trematoda: Digenea) en peces marinos de aguas Mexicanas. Anales del Instituto de Biología. Universidad Nacional Autonóma de México 23, 155165.Google Scholar
Cable, R.M. (1956) Opistholebes diodontis n. sp., its development in the final host, the affinities of some amphistomatous trematodes from marine fishes and the allocreadioid problem. Parasitology 46, 113.CrossRefGoogle Scholar
Cable, R.M. & Hunninen, A.V. (1942) Studies on Deropristis inflata (Molin), its life history and affinities to trematodes of the family Acanthocolpidae. Biological Bulletin 82, 292312.CrossRefGoogle Scholar
Cannon, L.R.G. (1978) Marine cercariae from the gastropod Cerithium moniliferum Kiener at Heron Island, Great Barrier Reef. Proceedings of the Royal Society of Queensland 89, 4557.Google Scholar
Cribb, T.H., Bray, R.A., Barker, S.C., Adlard, R.D. & Anderson, G.R. (1994) Ecology and diversity of digenean trematodes of the reef and inshore fishes of Queensland. International Journal for Parasitology 24, 851860.CrossRefGoogle ScholarPubMed
Cribb, T.H., Bray, R.A., Littlewood, D.T.J., Pichelin, S.P. & Herniou, E.A. (2001) The Digenea. pp. 168185in Littlewood, D.T.J. & Bray, R.A. (Eds) Interrelationships of the Platyhelminthes. London, Taylor & Francis.Google Scholar
Cribb, T.H., Bray, R.A., Olson, P.D. & Littlewood, D.T.J. (2003) Life cycle evolution in the Digenea: a new perspective from phylogeny. Advances in Parasitology 54, 198254.Google ScholarPubMed
Durie, P.H. (1956) The paramphistomes (Trematoda) of Australian ruminants III. The life-history of Calicophoron calicophorum (Fischoeder) Nasmark. Australian Journal of Zoology 4, 152157.CrossRefGoogle Scholar
Froese, R. & Pauly, D. (2004/2009) FishBase. World Wide Web electronic publication, available at www.fishbase.org, version 04/2009 (accessed January 2009).Google Scholar
Gibson, D.I. (1987) Questions in digenean systematics and evolution. Parasitology 95, 429460.CrossRefGoogle ScholarPubMed
Hall, K. & Chambers, C.B. (1999) A new genus of the Gyliauchenidae Goto et Matsudaira, 1918 (Digenea) from Naso tuberosus (Percomorpha, Acanthuridae) on the Great Barrier Reef, Queensland, Australia. Acta Parasitologica 44, 229232.Google Scholar
Hall, K. & Cribb, T.H. (2004) Ptychogyliauchen, a new genus of Gyliauchenidae (Platyhelminthes: Digenea) from siganid fishes of the Indo-West Pacific. Invertebrate Systematics 18, 607625.CrossRefGoogle Scholar
Hall, K. & Cribb, T.H. (2005) Family Gyliauchenidae Fukui, 1929. pp. 665678in Jones, A., Bray, R.A. & Gibson, D.I. (Eds) Keys to the Trematoda. Vol. 2. London, CABI Publishing and the Natural History Museum.Google Scholar
Hassanine, R.M. (2006) The life-cycle of Diploproctodaeum arothroni Bray & Nahhas, 1998 (Lepocreadiidae Odhner, 1905), with a comment on parasitic castration in its molluscan intermediate host. Journal of Natural History 40, 12111223.CrossRefGoogle Scholar
Jones, M.K., Hughes-Stamm, S.R., East, R.M. & Cribb, T.H. (2000) Ultrastructure of the digestive tract of Gyliauchen nahaensis (Platyhelminthes, Digenea), an inhabitant of the hindgut of herbivorous fishes. Journal of Morphology 246, 198211.3.0.CO;2-2>CrossRefGoogle ScholarPubMed
Køie, M. (1975) On the morphology and life-history of Opechona bacillaris (Molin, 1859) Looss, 1907 (Trematoda, Lepocreadiidae). Ophelia 13, 6386.CrossRefGoogle Scholar
Lengy, J. & Shchory, M. (1970) Studies on larval stages of digenetic trematodes in aquatic molluscs of Israel. I. On two cercariae encountered in the marine snails Littorina neritoides (L.) and Nassa circumcincta (Adams, 1851). Israel Journal of Zoology 19, 135144.Google Scholar
Littlewood, D.T.J., Cribb, T.H., Olson, P.D. & Bray, R.A. (2001) Platyhelminth phylogenetics – a key to understanding parasitism? Belgian Journal of Zoology 131, 3546.Google Scholar
Macfarlane, W.V. (1951) The life cycle of Stegodexamene anguillae n. g. n. sp., an allocreadiid trematode from New Zealand. Parasitology 41, 110.CrossRefGoogle Scholar
Manter, H.W. & Pritchard, M.H. (1962) Studies on digenetic trematodoes of Hawaiian fishes: Families Fellodistomatidae, Opistholebetidae and Gyliauchenidae. Transactions of the American Microscopical Society 81, 113123.CrossRefGoogle Scholar
Nagaty, H.F. (1956) Trematodes of fishes from the Red Sea. Part 7. On two gyliauchenids and three allocreadiids, including four new species. Journal of Parasitology 42, 523527.CrossRefGoogle Scholar
Nicoll, W. (1915) The trematode parasites of North Queensland. III. Parasites of fishes. Parasitology 8, 2241.CrossRefGoogle Scholar
Odening, K. (1974) Verwandtschaft, System und zykloontogenetische Besonderheiten Trematoden. Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie der Tiere 101, 345396.Google Scholar
Olson, P.D., Cribb, T.H., Tkach, V.V., Bray, R.A. & Littlewood, D.T.J. (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733755.CrossRefGoogle ScholarPubMed
Ozaki, Y. (1933) Telotrema caudatum n. g., n. sp., ein neuer Typus der Trematoden-Familie Gyliauchenidae (Goto et Matsudaira). Zoologische Anzeiger 103, 329332.Google Scholar
Ozaki, Y. (1934) Petalocotyle nipponica, a new type of the trematode family Allocreadiidae. Proceedings of the Imperial Academy (Tokyo) 10, 111114.CrossRefGoogle Scholar
Ozaki, Y. (1936) Flagellotrema convolutum, n. g., n. sp, a new trematode of the family Gyliauchenidae. Zoological Magazine, Tokyo 48, 951953.Google Scholar
Ozaki, Y. (1937) Studies on the trematode families Gyliauchenidae and Opistholebetidae, with special reference to lymph system. Journal of Science of the Hirosima University, series B 5, 43120.Google Scholar
Paggi, L. & Orecchia, P. (1963) Revisione della posizione sistematica di Distomum fracmm Rudolphi, 1819 e proposta di un nuovo genere Robphildollfusium gen. Parassitologia 5, 283296.Google Scholar
Palombi, A. (1937) Il ciclo biologico di Lepocreadium album Stossich sperimentalmente realizzato. Rivista di Parassitologia 1, 112.Google Scholar
Pearson, J.C. (1972) A phylogeny of life-cycle patterns of the Digenea. Advances in Parasitology 10, 153189.CrossRefGoogle ScholarPubMed
Pearson, J.C. (1992) On the position of the digenean family Heronimidae: an inquiry into a cladistic classification of the Digenea. Systematic Parasitology 21, 81166.CrossRefGoogle Scholar
Randall, J.E. (1983) Red Sea reef fishes. 2nd edn. 192 pp. London, IMMEL Publishing.Google Scholar
Shalaby, I.M. & Hassanine, R.M. (1997) Progyliauchen n. gen, n. sp. (Trematoda: Digenea) from the Red Sea fishes: as described by the light and scanning electron microscopy. Journal of the Egyptian–German Society of Zoology 22, 1527.Google Scholar
Sharabati, D. (1984) Red Sea shells. 2nd edn. 128 pp. London, KPI Ltd.Google Scholar
Stunkard, H.W. (1969) The morphology and life-history of Neopechona pyriforme (Linton, 1900) n. gen., n.comb. (Trematoda: Lepocreadiidae). Biological Bulletin 136, 96113.CrossRefGoogle Scholar
Stunkard, H.W. (1972) Observations on the morphology and life-history of the digenetic trematode, Lepocreadium setiferoides (Miller and Northup, 1926) Martin, 1938. Biological Bulletin 142, 326334.CrossRefGoogle ScholarPubMed
Stunkard, H.W. (1980a) The morphology, life-history and taxonomic relations of Lepocreadium areolatum (Linton, 1900) Stunkard, 1969 (Trematoda: Digenea). Biological Bulletin (Woods Hole) 158, 154163.CrossRefGoogle Scholar
Stunkard, H.W. (1980b) Successive hosts and developmental stages in the life history of Neopechona cablei sp. n. (Trematoda: Lepocreadiidae). Journal of Parasitology 66, 636641.CrossRefGoogle Scholar
Watson, R.A. (1984) The life cycle and morphology of Tetracerasta blepta, gen. et sp. nov., and Stegodexamene callista, sp. nov. (Trematoda: Lepocreadiidae) from the long-finned eel, Anguilla reinhardtii Steindacher. Australian Journal of Zoology 32, 177204.CrossRefGoogle Scholar
Yamaguti, S. (1934) Studies on the helminth fauna of Japan. Part 2. Trematodes of fishes. I. Japanese Journal of Zoology 5, 249541.Google Scholar
Yamaguti, S. (1942) Studies on the helminth fauna of Japan. Part 39. Trematodes of fishes mainly from Naha. Transactions of the Biogeographical Society of Japan 3, 329397.Google Scholar
Yamaguti, S. (1971) Synopsis of digenetic trematodes of vertebrates. 1074 pp. Tokyo, Keigaku Publishing Company.Google Scholar