Systematic Parasitology

, Volume 63, Issue 3, pp 201–219

Prosorhynchoides gracilescens (Rudolphi, 1819) (Digenea: Bucephalidae) from Lophius piscatorius L. is a species complex: a redescription of this species (sensu stricto) from the western Mediterranean and the description of P. borealis n. sp. from the northern North-East Atlantic

  • Pierre Bartoli
  • David I. Gibson
  • Rodney A. Bray
Article

Abstract

The bucephalid digenean Prosorhynchoides gracilescens (Rudolphi, 1819) is a common intestinal parasite of the angler fish Lophius piscatorius in European marine waters. Detailed studies of new material collected off the coasts of both Marseilles and Corsica in the western Mediterranean, and comparison with museum material from the northern North-East Atlantic, indicated that the accepted concept of this species comprises two distinct taxa. The Mediterranean form occurs in relatively small numbers and has small eggs, a large rhynchus and a vitelline distribution that finishes well short of the rhynchus, whereas the NE Atlantic form, which comprises the majority of records, occurs often in large numbers, has larger eggs, a relatively smaller rhynchus and a vitelline distribution that tends to reach the rhynchus. Since the type-material is from the Mediterranean and resembles the Mediterranean form, there was little option but to consider the latter as P. gracilescens (sensu stricto) and to describe the NE Atlantic form as a new species, for which the name P. borealis n. sp. is coined to reflect its northerly distribution. Both species are described and figured in detail, and a table and illustration of the diagnostic features are presented. In addition, some discussion is included on the distribution of these two species and whether P. gracilescens (s. str.) might be a relict species, and on non-European records of P. gracilescens (sensu lato).

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Afonso-Dias, I. & MacKenzie, K. (2002) Gastrointestinal parasites of Northeast Atlantic anglerfish (Lophius spp.) as biological tags: a pilot study. In: Abstracts of the Tenth International Congress of Parasitology, Vancouver, Canada, 4–9 August, 2002, p. 266Google Scholar
  2. Baylis H.A. (1939) Further records of parasitic worms from British vertebrates. Annals and Magazine of Natural History, Series 11, 4, 473–498Google Scholar
  3. Baylis H.A, Jones E.I. (1933) Some records of parasitic worms from marine fishes at Plymouth. Journal of the Marine Biological Association of the United Kingdom 18, 627–634Google Scholar
  4. Bona F., Buriola E., Cerioni S., Di Cave D., Orecchia P., Paggi L. (1995). Digenea. In: Minell A., Ruffo S., La Posta, S. (eds). Checklist della specie della Fauna Italiana. Fascicolo 5. Edizioni Calderini, Bologna, 31 pp.Google Scholar
  5. Bray R.A. (1973) Some digenetic trematodes in fishes from the Bay of Biscay and nearby waters. Bulletin of the British Museum (Natural History), Zoology 26, 151–183Google Scholar
  6. Briggs J.C. (1974) Marine zoogeography. New York: McGraw-Hill Book Company, 475 ppGoogle Scholar
  7. Brinkmann A., Jr (1957) Fish trematodes from Norwegian waters. IIa. The Norwegian species of the orders Aspidogastrea and Digenea (Gasterostomata). Arbok for Universitetet i Bergen 4, 1–29, 2plsGoogle Scholar
  8. Caruso J.H. (1986) Lophiidae. In: Whitehead P.J.P., et al. (Ed.), Fishes of the North-eastern Atlantic and the Mediterranean Paris: UNESCO, Vol. 3, pp. 1362–1363Google Scholar
  9. Cobbold T.S. (1858) XII. Observations on Entozoa, with notices of several species, including an account of two experiments in regards to the breeding of Taenia serrata and T. cucumerina. Transactions of the Linnean Society of London 22:155–172Google Scholar
  10. Cordero del Campillo M., Ordonez L.C., Feo A.R. (1994) Indice-catalogo de zooparasitos ibericos. Léon: Universidad de Léon, Secretariado de Publicaciones, 650 ppGoogle Scholar
  11. Dawes B. (1947) The Trematoda of British fishes. London: Ray Society, 364 ppGoogle Scholar
  12. Dawes B. (1968) The Trematoda with special reference to British and other European forms. Cambridge: Cambridge University Press, 644 ppGoogle Scholar
  13. Diesing K.M. (1858) Revision der Myzhelminthen, Abteilung: Trematoden. Sitzungsberichte der Kaiser Akademie Wissenschaften. Mathematisch-Naturwissenschaftliche Classe, Wien 32(23), 307–390Google Scholar
  14. Dollfus, R.P. (1953) Aperçu général sur l’histoire naturelle des parasites animaux de la morue Atlanto-Arctique Gadus callarias L. (=morhua). Paris: Lechevalier. Encyclopédie Biologique, 43, 423 ppGoogle Scholar
  15. Duniec H. (1980) Parasitic fauna of the grey gurnard Trigla gurnardus (L.) from Shetland Islands fishing grounds. Acta Ichthyologica et Piscatoria, 10, 65–77Google Scholar
  16. Eckmann F. (1932) Beiträge zur kenntnis der trematodenfamilie Bucephalidae. Zeitschrift für Parasitenkunde 5, 94–111CrossRefGoogle Scholar
  17. Ekman S. (1967) Zoogeography of the sea. London: Sidgwick & Jackson, 417 ppGoogle Scholar
  18. Erwin B.E., Halton D.W. (1983) Fine structural observations on spermatogenesis in a progenetic trematode, Bucephaloides gracilescens. International Journal for Parasitology 13, 413–426CrossRefGoogle Scholar
  19. Eydal M., Bambir S.H., Helgason S., Olafsdottir D. (1996) Prosorhynchoides (Bucephaloides) gracilescens (Digenea) in fish from Icelandic waters. Parassitologia 38, 33Google Scholar
  20. Eydal M., Bambir S.H., Helgason S., Olafsdottir D. (1998) Prosorhynchoides gracilescens (Digenea) in fish from Icelandic waters. Parasitology International 47(Suppl.), 302Google Scholar
  21. Eydal M., Helgason S., Kristmundsson A., Bambir S.H. (1999) Metacercariae (Digenea) in Atlantic cod, haddock, whiting and saithe around Iceland. Bulletin of the Scandinavian Society for Parasitology 9(1), 31–32Google Scholar
  22. Eydal M., Olafsdottir D. (2003) Intestinal macroparasites in anglerfish (Lophius piscatorius L.) from Icelandic waters. Bulletin of the Scandinavian Society for Parasitology 12-13:60–68Google Scholar
  23. Feral J.P. (2002) How useful are genetic markers in attempts to understand and manage marine biodiversity? Journal of Experimental Marine Biology and Ecology 268, 121–145CrossRefGoogle Scholar
  24. Froese, R. & Pauly D. (Eds.) (2004) FishBase. World Wide Web electronic publication. www.fishbase.org, version (11/2004)Google Scholar
  25. Gaevskaya A.V., Aleshkina L.D. (1985) New species of trematodes from the eastern Atlantic. Parazitologiya 19, 105–112. (In Russian)Google Scholar
  26. Gaevskaya A.V., Korniychuk Y.M. (2003) [Parasites organisms as a component of ecosystems of the Black Sea near-shore zone of Crimea]. In: V.N. Eremeev, Gaevskaya A.V. (eds). Modern condition of biologicala diversity in near-shore zone of Crimea (the Black Sea sector). NAS Ukraine Institute of Biology of the Southern Seas. EKOSI-Gidrophizika, Sevastopol, pp. 425–490. (In Russian)Google Scholar
  27. Gibson, D.I. (1996) Trematoda. In: Margolis L. & Kabata Z. (Eds) Guide to the parasites of fishes of Canada. Part IV. Canadian Special Publication of Fisheries and Aquatic Sciences No. 124. Ottawa: NRC Press, 373 ppGoogle Scholar
  28. Gibson D.I., Costa G. (1997) Helminth parasites of Madeiran rockpool fishes, with a redescription of Schikhobalotrema longivesiculatum Orecchia & Paggi, 1975 (Digenea: Haplosplanchnidae), and some comments on their zoogeographical relationships. Systematic Parasitology 38,73–79CrossRefGoogle Scholar
  29. Gibson D.I., Køie M. (1991) Magnibursatus caudofilamentosa (Reimer, 1971) n. comb. (Digenea: Derogenidae) from the stickleback Gasterosteus aculeatus L. in Danish waters: a zoogeographical anomaly? Systematic Parasitology 20, 221–228CrossRefGoogle Scholar
  30. Greze V.N., Delyamure S.L., & Nikolaeva V.M. (Ed.) (1975) [Identification keys to the parasites of vertebrates from the Black and Azov Seas. Parasitic invertebrates of fishes, fish-eating birds and marine mammals]. Kiev: Naukova Dumka, 551 pp. (In Russian)Google Scholar
  31. Halton D.W., Johnston B.R. (1982) Occurrence and infectivity of Bucephaloides gracilescens (Trematoda: Bucephalidae) in angler fish from the Irish Sea. Irish Naturalists Journal 20:526–531Google Scholar
  32. Hartwich G., Kilias I. (1990) Die Trematoden-Typen des Zoologischen Museum in Berlin. Mitteilungen aus dem Zoologischen Museum in Berlin 66, 125–176Google Scholar
  33. Hopkins S.H. (1954) The American species of trematode confused with Bucephalus (Bucephalopsis) haimeanus. Parasitology 44, 353–370PubMedGoogle Scholar
  34. Jennings M.R., Hendrickson G.L. (1982) Parasites of chinook salmon (Oncorhynchus tshawytscha) and coho salmon (O. kisutch) from the Mad River and vicinity, Humboldt County, California. Proceedings of the Helminthological Society of Washington 49, 279–284Google Scholar
  35. Johnstone J. (1905) Internal parasites and diseased conditions of fishes. Proceedings and Transactions of the Liverpool Biological Society, 19, 278–300, pl. III–VIGoogle Scholar
  36. Køie M. (1985) The surface topography and life-cycles of digenetic trematodes in Limanda limanda (L.) and Gadus morhua L. (Summary). Naturvidenskabelige Doktorgrad. Naturvidenskabelige Fakultet ved Kobenhavns Universitet, 20pp. + 1plGoogle Scholar
  37. Køie M. (2000) Metazoan parasites of teleost fishes from Atlantic waters off the Faroe Islands. Ophelia 52, 25–44Google Scholar
  38. Kostadinova A.K., Power A.M., Fernandez M., Balbuena J.A., Raga J.A., Gibson D.I. (2003) Three species of Magnibursatus Naidenova, 1969 (Digenea: Derogenidae) from Atlantic and Black Sea marine teleosts. Folia Parasitologica 50:202–210PubMedGoogle Scholar
  39. Lebour M.V. (1908) Fish trematodes of the Northumberland coast. Northumberland Sea Fisheries Report for 1907, pp. 1–47, 5plGoogle Scholar
  40. Linton E. (1905) Parasites of fishes of Beaufort, North Carolina. Bulletin of the Bureau of Fisheries 24:321–428Google Scholar
  41. Linton E. (1910) Helminthfauna of the Dry Tortugas, II. Trematodes. Papers from the Tortugas Laboratory of the Carnegie Institute of Washington 4, 11–98Google Scholar
  42. Linton E. (1940) Trematodes from fishes mainly from the Woods Hole region, Massachusetts. Proceedings of the United States National Museum, 88, 1–172, 26 plGoogle Scholar
  43. Littlewood D.T.J., Rohde K., Clough K.A. (1998) The phylogenetic position of Udonella (Platyhelminthes). International Journal for Parasitology 28, 1241–1250PubMedCrossRefGoogle Scholar
  44. Love M.S. & Moser M. (1983) A checklist of parasites of California, Oregon, and Washington marine and estuarine fishes. NOAA Technical Report NMFS SSRF, 777, 577 ppGoogle Scholar
  45. Manter H.W. (1931) Some digenetic trematodes of marine fishes of Beaufort, North Carolina. Parasitology 23:396–411Google Scholar
  46. Mathias P. (1934) Sur quelques trématodes de poissons marins de la région de Banyuls. Archives de Zoologie Expérimentale et Générale 75:567–581Google Scholar
  47. Matthews R.A. (1974) The life cycle of Bucephaloides gracilescens (Rudolphi, 1819) Hopkins, 1954 (Digenea: Gasterostomata). Parasitology 68:1–12PubMedGoogle Scholar
  48. Mola P. (1928) Vermi parassiti dell’ittiofauna Italiana. Bolletino di Pesca, di Piscicoltura e di Idriobiologica 4: 395–443Google Scholar
  49. Molin R. (1859). Nuovi myzelmintha raccolti ed esaminati. Sitzungsberichte der Kaiserlichen der Wissenschaften. Mathematisch-Naturwissenschaftliche Classe 37: 818–854, + 3 plGoogle Scholar
  50. Muñoz M.V., Fernandez J.P., Carbonell E., Orts M.E. (1989) Contribucion al estudio de algunos bucefalides (Trematoda: Bucephalidae) parasitos de peces marinos de aguas ibericas. Revista Iberica de Parasitologia 49, 27–35Google Scholar
  51. Nagaty, H.F. (1937) Trematodes of fishes from the Red Sea. Part I. Studies on the family Bucephalidae, Poche, 1907. Cairo: Egyptian University, Faculty of Medicine Publication No. 12, 172 ppGoogle Scholar
  52. Nicoll W. (1909) A contribution towards a knowledge of the entozoa of British marine fishes. Part II. Annals and Magazine of Natural History, Series 8, 4, 1–25Google Scholar
  53. Nicoll W. (1913) Trematode parasites from food fishes of the North Sea. Parasitology 6:188–194CrossRefGoogle Scholar
  54. Nicoll W. (1914) The Trematodes parasites of fishes from the English Channel. Journal of the Marine Biological Association of the United Kingdom 10:466–505CrossRefGoogle Scholar
  55. Nicoll W. (1915) A list of the trematode parasites of British marine fishes. Parasitology 7:339–378Google Scholar
  56. 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, 733–755PubMedCrossRefGoogle Scholar
  57. Olsson P. (1868) Entozoa, iakttagna hos Skandinaviska hafsfiskar. Lunds Universitets Årsskrift 4, 64pp.Google Scholar
  58. Olsson P. (1876) Entozoa, iakttagna hos Skandinaviska hafsfiskar, II. Lunds Universitets Årsskrift 14:25pp.Google Scholar
  59. Orecchia P., Paggi L. (1978) Aspetti di sistematica e di ecologia degli elminti parassiti di pesci marini studiati presso l’Istituto di Parassitologia dell’Università di Roma. Parassitologia 20:73–89PubMedGoogle Scholar
  60. Orlowska K. (1979) Parasites of North Sea spiny dogfish, Squalus acanthias L. (Selachiiformes, Squalidae). Acta Ichthyologica et Piscatoria 9:33–44Google Scholar
  61. Osmanov S.U. (1940) [Studies on the parasite fauna of fish of the Black Sea.] Uchenye Zapiski Leningradskogo Gosudarstvennogo. Pedagogicheskogo Inst Imeni A.I. Gertsena 30, 187–265 (In Russian)Google Scholar
  62. Overstreet R.M., Curran S.S. (2002) Superfamily Bucephaloidea Poche 1907. In: Gibson D.I., Jones A., Bray R.A. (Eds) Keys to the Trematoda. Wallingford: CABI Publishing and The Natural History Museum, Vol. 1, pp. 67–110.Google Scholar
  63. Papoutsoglou S.E. (1976) Metazoan parasites of fishes from Saronicos Gulf Athens-Greece. Thalassographica 1:69–102Google Scholar
  64. Parukhin A.M. (1966). On the species composition of the helminth fauna of fishes in the South Atlantic. Materialy Nauchnoi Konferentsii Vsesoyuznogo Obshchestva Gel’mintologov 3, 219–222 (In Russian)Google Scholar
  65. Parukhin A.M. (1968) Helminth fauna of fish in the South Atlantic. In: Bodyanitski V.A. (Ed.) Biology of the seas. No. 14. Parasites of marine animals. Naukova Dumka, Kiev, pp. 96–113 (In Russian)Google Scholar
  66. Parukhin A.M. (1978). [On studies in trematodofauna of the Indian and Atlantic Ocean fishes]. Biologiya MoryaKiev 45:90–99, In Russian)Google Scholar
  67. Parukhin A.M. (1989). [Parasitic worms of bottom fishes of the Southern Seas]. Naukova Dumka, Kiev, 156 pp. (In Russian)Google Scholar
  68. Reimer L.W. (1985) Bucephalidae (Digenea) aus Fischen der Küste von Moçambique. Angewandte Parasitologie 26: 13–26Google Scholar
  69. Renaud F., Blanquer A., Gabrion C. (1990) Genetic divergence in Bothriocephalus gregarius: a hypothesis based on the paleogeographic movements of their teleost (Psetta) hosts. International Journal for Parasitology 20:637–643CrossRefGoogle Scholar
  70. Rudolphi C.A. (1819). Entozoorum synopsis, cui accidunt mantissa duplex et indices locupletissimi. Sumtibus Augusti Rücker, Berolini, 811 pp. + 3 platesGoogle Scholar
  71. Sey, O. (1970) Parasitic helminths occurring in Adriatic fishes. Part II. (Flukes and tapeworms). Acta Adriatica, 13(6): 3–15.Google Scholar
  72. Skrjabin, K.I. & Guschanskaja, L.K. (1962) [Order Bucephalida (Odening, 1960) Skrjabin et Guschanskaja.] In:␣Skrjabin, K.I. (Ed.) [Trematodes of animals and man.] Osnovy Trematodologii, 20, 165–563 (In Russian)Google Scholar
  73. Srivastava C.B., Chauhan B.S. (1973) A review of Indian gasterostomes (Trematoda). Records of the Zoological Survey of India 67:1–13Google Scholar
  74. Stewart M., Marks N.J., Halton D.W. (2003) Neuroactive substances and associated major muscle systems in Bucephalopsis gracilescens (Trematoda: Digenea) metacercaria and adult. Parasitology Research 91:12–21PubMedCrossRefGoogle Scholar
  75. Stossich M. (1890) Brani di elminthologia tergestina. Serie settima. Bolletino della Società Adriatica di Scienze Naturali in Trieste 12:39–47Google Scholar
  76. Stunkard H.W. (1973) Gasterostome trematodes of the Woods Hole region. Biological Bulletin. Marine Biological Laboratory Woods Hole 145:456–457CrossRefGoogle Scholar
  77. Stunkard H.W. (1974) The life-cycle of the gasterostome trematodes, Rhipidocotyle transversale Chandler, 1935 and Rhipidocotyle lintoni Hopkins, 1954. Biological Bulletin. Marine Biological Laboratory Woods Hole 147:500–501Google Scholar
  78. Stunkard H.W. (1976) The life cycles, intermediate hosts, and larvae of Rhipidocotyle transversale Chandler, 1935 and Rhipidocotyle lintoni Hopkins, 1954: life-cycles and systematics of bucephalid trematodes. Biological Bulletin. Marine Biological Laboratory Woods Hole 150:294–317CrossRefGoogle Scholar
  79. Thompson M., Halton D.W. (1982) The surface morphology of a gasterostome trematodeBucephaloides gracilescens. Parasitology 84(1): lxxiiGoogle Scholar
  80. Ungaro N., Marano G., Auteri R., Voliani A., Massuti E., García-Rodríguez M., Omsnai K. (2002) Distribution, abundance and biological features of anglerfish (Lophius piscatorius and Lophius budegassa) (Osteichthyes: Lophiiformes) in the Mediterranean Sea. Scientia Marina 66 (Suppl. 2), 55–63Google Scholar
  81. Viudez A., Tintore J., Haney R.L. (1996) Circulation in the Alboran Sea as determined by quasi-synoptic hydrographic observations. Part 1: Three-dimensional structure of the two anticyclonic gyres. Journal of Physical Oceanography 26: 684–705CrossRefGoogle Scholar
  82. Wagener G.R. (1852) Enthelminthica. No. II. Ueber eine Distomengattung Gasterostoma v. Siebold. Archiv für Anatomie, Physiologie und Wissenschaftliche Medicin 1852: 557–569Google Scholar
  83. Williams H.H. (1960) A list of parasitic worms, including 22 new records, from marine fishes caught off the British Isles. Annals and Magazine of Natural History, Series 13, 2, 705–715Google Scholar
  84. Yamaguti, S. (1971) Synopsis of the digenetic trematodes of vertebrates. Tokyo: Keigaku Publlishing Co., Vol. 1, 1074 pp., Vol. 2, 349 pls.Google Scholar
  85. Zernov S.A. (1913) Materiaux pour la biologie de la Mer Noire. Memoires de l’Academie Impériale des Sciences de St. Petersbourg. Classe des Sciences, Physiques et Mathématique, 8th Series, 32, 1–299. (In Russian).Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Pierre Bartoli
    • 1
  • David I. Gibson
    • 2
  • Rodney A. Bray
    • 2
  1. 1.Centre d’Océanologie de Marseille, UMR 6540 du CNRS, DIMARCampus Universitaire de LuminyMarseille cédex 9France
  2. 2.Department of ZoologyThe Natural History MuseumLondonUK

Personalised recommendations