Skip to main content Skip to main navigation menu Skip to site footer
Type: Articles
Published: 2012-12-10
Page range: 58–70
Abstract views: 42
PDF downloaded: 3

The discovery of progenetic Allocreadium neotenicum Peters, 1957 (Digenea: Allocreadiidae) in water beetles (Coleoptera: Dytiscidae) in Great Britain

Department of Life Sciences, Natural History Museum, Cromwell Road, London, SW7 5BD, England
The Aquatic Coleoptera Conservation Trust, 3 Eglinton Terrace, Ayr KA7 1JJ, Scotland
Department of Life Sciences, Natural History Museum, Cromwell Road, London, SW7 5BD, England
Department of Life Sciences, Natural History Museum, Cromwell Road, London, SW7 5BD, England
Coleoptera Pseudallocreadium Hydroporus Agabus England Scotland

Abstract

Progenetic specimens of Allocreadium neotenicum Peters, 1957 are described from water beetles, Hydroporus rufifrons, an endangered species, and Agabus paludosus from northern England and Scotland, and as non-ovigerous metacercariae from Agabus melanarius from southern England. Morphologically, the worms are identical to A. neotenicum described from water beetles in North America. Molecular phylogenetic estimates based on 28S rDNA sequences show these British specimens as more closely related to the North American freshwater fish parasite Allocreadium lobatum Wallin, 1909 than to the European species A. isoporum (Looss, 1894). A. lobatum shows a predilection for progenesis and may be a senior synonym of A. neotenicum. Based on the molecular phylogeny, the genus Pseudallocreadium Yamaguti, 1971 is considered synonymous with Allocreadium and the two species assigned to that genus, P. neotenicum and P. alloneotenicum (Wootton, 1957) are returned to Allocreadium.

References

  1. Auwera, G. van der, Chapelle, S. & de Wachter, R. (1994) Structure of the large ribosomal subunit RNA of Phytophthora megasperma, and phylogeny of the oomycetes. FEBS Letters, 338, 133–136.

    Caira, J.N. & Bogéa, T. (2005) Family Allocreadiidae Looss, 1902. In: Jones, A., Bray, R.A. & Gibson, D.I. (Eds), Keys to the Trematoda. Volume 2. CABI Publishing and the Natural History Museum, Wallingford, pp. 417–436.

    Caira, J.N. & Scudder, G.G.E. (1985) Pseudoallocreadium alloneotenicum (Wootton, 1957) Yamaguti, 1971 (Digenea: Allocreadiidae) from Psychoglypha alascensis Banks (Trichoptera: Limnephilidae) in Vancouver, British Columbia. Journal of Parasitology, 71, 524. doi:10.2307/3281555.

    Camp, J.W. (1989) Population biology of Allocreadium lobatum (Trematoda: Allocreadiidae) in Semotilus atromaculatus. American Midland Naturalist, 122, 236–241.

    Camp, J.W. (1992) Occurrence of Allocreadium neotenicum in aquatic hosts from northern Indiana. American Midland Naturalist, 128, 203–208. doi: 10.2307/2426426.

    Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17, 540–552.

    Choudhury, A., Daverdin, R.H. & Brooks, D.R. (2002) Wallinia chavarriae n. sp. (Trematoda: Macroderoididae) in Astyanax aeneus (Günther, 1860) and Bryconamericus scleroparius (Regan, 1908) (Osteichthyes: Characidae) from the Area de Conservación Guanacaste, Costa Rica. Journal of Parasitology, 88, 107–112.

    Crawford, W.W. (1940) An unusual case of a sexually mature trematode from the body cavity of a diving beetle. Journal of Parasitology, 26, Suppl., 32.

    DeGiusti, D.L. (1962) Ecological and life history notes on the trematode Allocreadium lobatum (Wallin, 1909) and its occurrence as a progenetic form in amphipods. Journal of Parasitology, 48 Sect. 2, 22.

    Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.

    Elwood, H.J., Olsen, G.J. & Sogin, M.L. (1985). The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. Molecular Biology and Evolution, 2, 399–410.

    Foster, G.N. (2010). A review of the scarce and threatened Coleoptera of Great Britain. Part 3: water beetles. Species Status No. 1, Joint Nature Conservation Committee, Peterborough. 143 pp.

    Foster, G.N., Bilton, D.T., Routledge, S. & Eyre, M.D. (2008). The past and present statuses of Hydroporus rufifrons (Müller) (Coleoptera, Dytiscidae) in Great Britain. The Coleopterist, 17, 51–63.

    Foster, G.N. & Friday, L.E. (2011). Keys to adults of the water beetles of Britain and Ireland (Part I). (Coleoptera: Hydradephaga: Gyrinidae, Haliplidae, Paelobiidae, Noteridae and Dytiscidae). Handbooks for the Identification of British Insects Vol. 4 Part 3 (2nd Ed.). St Albans: Royal Entomological Society. 144 pp.

    Gibson, D.I. (1996) Trematoda. In: Margolis, L. & Kabata, Z. (Eds) Guide to the parasites of fishes of Canada, Part IV. NRC Research Press, Canadian Special Publication of Fisheries and Aquatic Sciences, Ottawa 124, pp. 1–373.

    Gould, S.J. (1977) Ontogeny and phylogeny. The Belknap Press of Harvard University Press, Cambridge, Massachusetts. 501 pp.

    Gouy, M., Guindon, S. & Gascuel, O. (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution, 27, 221–224.

    Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59, 307–321.

    Herrmann, K.K. & Poulin, R. (2012) Geographic variation in life cycle strategies of a progenetic trematode. Journal of Parasitology, 98, 103-110. doi: 10.1645/GE-2789.1.

    Holopainen, I.J., Lamberg, S., Valtonen, E.T. & Rantanen, J. (1997) Effects of parasites on the life history of the freshwater bivalve, Pisidium amnicum, in eastern Finland. Archiv für Hydrobiologie, 139, 461–477.

    Hopkins, S.H. (1931) Studies on Crepidostomum. II. The "Crepidostomum laureatum" of A. R. Cooper. Journal of Parasitology, 18, 79–91.

    Jackson, D.J. (1958) Notes on some nematodes and trematodes infesting water beetles. Entomologist's Monthly Magazine, 94, 109–111.

    Jiménez-Guzmán, F. (1973) Trematodos digeneos de peces dulceacuícolas de Nuevo León, México. I. Dos nuevas especies y un registro nuevo en el caracido Astyanax fasciatus mexicanus (Filippi). Cuadernos del Instituto de Investigaciones Cientificos, Universidad Autónoma de Nuevo León, México, 17, 1–19.

    Lamothe-Argumedo, R. (1970) Tremátodos de peces VI. Margotrema bravoae gen., nov., sp., nov., (Trematoda: Allocreadiidae) parásito de Lermichthys multiradiatus Meek. Anales del Instituto de Biología, Universidad Nacional Autónoma de México, 41, 87–92.

    Larson, D.J., Alarie, Y. & Roughley, R.E. (2000). Predaceous diving beetles (Coleoptera: Dytiscidae) of the Nearctic Region, with emphasis on the fauna of Canada and Alaska. National Research Council of Canada Research Press, Ottawa. 982 pp.

    Lefebvre, F. & Poulin, R. (2005) Progenesis in digenean trematodes: a taxonomic and synthetic overview of species reproducing in their second intermediate hosts. Parasitology, 130, 587–560. doi: 10.1017/S0031182004007103.

    Littlewood, D.T.J., Curini-Galletti, M. & Herniou, E.A. (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution, 16, 449–466.

    Littlewood, D.T.J. & Olson, P.D. (2001) SSU rDNA and the Platyhelminthes: signal, noise, conflict and compromise. In: Littlewood, D.T.J., & Bray, R.A. (Eds) Interrelationships of the Platyhelminthes. Taylor & Francis, London, pp. 262–278.

    Littlewood, D.T.J., Waeschenbach, A. & Nikolov, P.N. (2008) In search of mitochondrial markers for resolving the phylogeny of cyclophyllidean tapeworms (Platyhelminthes, Cestoda) – a test study with Davaineidae. Acta Parasitologica, 53, 133–144.

    Looss, A. (1894) Die Distomen unserer Fische und Frösche. Neue Untersuchungen über Bau und Entwicklung des Distomenkörpers. Bibliotheca Zoologica, 16, 1–296.

    Looss, A. (1900) Nachträgliche Bemerkungen zu den Namen der von mir vorgeschlagenen Distomidengattungen. Zoologischer Anzeiger, 23, 601–608.

    Looss, A. (1902) Über neue und bekannte Trematoden aus Seeschildröten. Nebst Erörterungen zur Systematik un Nomenclatur. Zoologische Jahrbücher. Abteilung für Systematik Okologie und Geographie der Tiere, 16, 411–894.

    Margolis, L. & Arthur, J.R. (1979) Synopsis of the parasites of fishes of Canada. Bulletin of the Fisheries Research Board of Canada, 199, 1–269.

    Mueller, J.F. (1934) Parasites of Oneida Lake fishes. Part IV. Additional notes on parasites of Oneida Lake fishes, including descriptions of new species. Roosevelt Wild Life Annals, 3, 335–373.

    Müller, O.F. (1776) Zoologiæ Danicæ prodromus seu animalium Daniæ et Norvegiæ indigenarum characteres, nomina et synonyma imprimis popularium. Impensis Auctoris, Havniæ. 282 pp.

    Muzzall, P.M. (1981) Parasites of the isopod, Caecidotea communis, and amphipod, Hyalella azteca,in New Hampshire. Proceedings of the Helminthological Society of Washington, 48, 91–92.

    Muzzall, P.M. (1982) Parasites of Gammarus pseudolimnaeus and Hyalella azteca (Crustacea: Amphipoda) in three south-central Michigan localities. Proceedings of the Helminthological Society of Washington, 49, 289–294.

    Niewiadomska, K. & Valtonen, E.T. (2007) Morphology, development and probable systematic position of Cercariaeum crassum Wesenberg-Lund, 1934 (Digenea), a parasite of Pisidium amnicum in eastern Finland. Systematic Parasitology, 68, 147–154. doi 10.1007/s11230-007-9093-7.

    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, 733–755.

    Pandey, K.C. & Agrawal, N. (1977) A progenetic metacercaria of Allocreadium sp., from a dragon fly nymph. Indian Journal of Parasitology, 1, 123–124.

    Pearse, A.S. (1924) Observations on parasitic worms from Wisconsin fishes. Transactions of the Wisconsin Academy of Sciences, Arts and Letters, 21, 147–160.

    Peters, L.E. (1955) Morphology of the adult and the miracidium of a progenetic species of Allocreadium from water beetles of the family Dytiscidae. Journal of Parasitology, 41, Suppl., 36.

    Peters, L.E. (1957) An analysis of the trematode genus Allocreadium Looss with the description of Allocreadium neotenicum sp. nov. from water beetles. Journal of Parasitology, 43, 136–142. doi:10.2307/3274638.

    Peters, L.E. & LaBonte, R.P. (1965) Comparative morphology of four species of allocreadiid miracidia (Trematoda). Journal of Parasitology, 51, 583–586.

    Petkevičiūtė, R., Stunžėnas, V. & Stanevičiūtė, G. (2012) Clarification of the systematic position of Cercariaeum crassum Wesenberg-Lund, 1934 (Digenea), based on karyological analysis and DNA sequences. Journal of Helminthology, 86, 293–301. doi:10.1017/S0022149X11000393.

    Rantanen, J.T., Valtonen, E.T. & Holopainen, I.J. (1998) Digenean parasites of the bivalve mollusc Pisidium amnicum in a small river in eastern Finland. Diseases of Aquatic Organisms, 33, 201–208.

    Reyda, F.B. & Olson, P.D. (2003) Cestodes of cestodes of Peruvian freshwater stringrays. Journal of Parasitology, 89, 1018–1024.

    Rudolphi, C.A. (1819) Entozoorum synopsis, cui accedunt mantissa duplex et indices locupletissimi. Sumtibus Augusti Rücker, Berolini. 811 pp.

    Siddiqi, M.N. (1981) Helminth parasites of fishes of northern Colorado. Biologia (Lahore), 27, 75–79.

    Stafford, E.W. (1932) Platyhelmia in aquatic insects and Crustacea. Journal of Parasitology, 18, 131.

    Surber, E.W. (1928) Megalogonia ictaluri, a new species of trematode from the channel cat-fish, Ictalurus punctatus. Journal of Parasitology, 14, 269.

    Szidat, L. (1943) Die Fischtrematoden der Gattung Asymphylodora Looss, 1899 und Verwandte. Zeitschrift für Parasitenkunde, 13, 25–61.

    Tkach, V.T., Littlewood, D.T.J., Olson, P.D., Kinsella, M.J. & Swiderski, Z. (2003). Molecular phylogenetic analysis of the Microphalloidea Morozov, 1955 (Trematoda: Digenea): a bigger data set resolves fewer genera. Systematic Parasitology, 56, 1–15.

    Telford, M.J., Lockyer, A.E., Cartwright-Finch, C. & Littlewood, D.T.J. (2003) Combined large and small subunit ribosomal RNA phylogenies support a basal position of the acoelomorph flatworms. Proceedings of the Royal Society B: Biological Sciences, 270, 1077–1083.

    Wallin, I.E. (1909) A new species of the trematode genus Allocreadium, with a revision of the genus and a key to the sub-family Allocreadiinae. Transactions of the American Microscopical Society, 29, 50–66.

    Wesenberg-Lund, C. (1934) Contributions to the development of the Trematoda Digenea. Part II. The biology of the freshwater cercariae in Danish freshwaters. Mémoires de l’Académie Royale des Sciences et des Lettres de Danemark, Copenhagen, Section des Sciences, 9me série, 5, 1–223, pl. 1–35.

    Willis, M.S. (2002) Morphological variation of Allocreadium lobatum (Digenea: Allocreadiidae) in the creek chub, Semotilus atromaculatus (Osteichthys: Cyprinidae), in Nebraska, USA. Transactions of the Nebraska Academy of Sciences, 28, 21–27.

    Wootton, D.M. (1957) Studies on the life-history of Allocreadium alloneotenicum sp. nov. (Allocreadiidae – Trematoda). Biological Bulletin, 113, 302–315.

    Yamaguti, S. (1971) Synopsis of digenetic trematodes of vertebrates. Keigaku, Tokyo, Vol. I, 1074 pp.; Vol. II, 349 pp.

    Zimbaluk, A.K. & Roitman, V.A. (1966) Trematode Bunodera mediovitellata parasite of stickleback in Commodore Islands. Trudy Gel'mintologicheskoi Laboratorii, 17, 290–296. (In Russian).