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Morphological and molecular characterization of tetraphyllidean merocercoids (Platyhelminthes: Cestoda) of striped dolphins (Stenella coeruleoalba) from the Western Mediterranean

Published online by Cambridge University Press:  18 November 2004

C. AGUSTÍ
Affiliation:
Marine Zoology Unit, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, P.O. Box 22085, 46071 Valencia, Spain
F. J. AZNAR
Affiliation:
Marine Zoology Unit, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, P.O. Box 22085, 46071 Valencia, Spain
P. D. OLSON
Affiliation:
Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
D. T. J. LITTLEWOOD
Affiliation:
Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
A. KOSTADINOVA
Affiliation:
Marine Zoology Unit, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, P.O. Box 22085, 46071 Valencia, Spain Department of Biodiversity, Central Laboratory of General Ecology, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113 Sofia, Bulgaria
J. A. RAGA
Affiliation:
Marine Zoology Unit, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, P.O. Box 22085, 46071 Valencia, Spain

Abstract

Two types of tetraphyllidean merocercoids, Phyllobothrium delphini and Monorygma grimaldii, are well known from most cetaceans world-wide. The role of cetaceans in the life-cycle of these merocercoids is unclear because their specific identity is as yet unknown. The problem is compounded by poor descriptions of both merocercoids. We used light and scanning electron microscopy, and histological techniques to provide a thorough description of merocercoids collected from 11 striped dolphins, Stenella coeruleoalba, from the Spanish Mediterranean. We also described, for the first time, specimens of P. delphini with immature proglottides. Our merocercoids were morphologically similar to those described previously, except in the structure of the apical organ. Intra- and inter-sample variability in the morphology of the apical organ suggested that it degenerates during larval development. A subsample of 16 specimens of P. delphini and M. grimaldii was characterized for the D2 variable region of the large subunit ribosomal RNA gene (LSU) and compared with published tetraphyllidean cestode LSU sequences. P. delphini showed 2 unique signatures that differed from one another by a single base, whereas all sequences of M. grimaldii were identical. This suggests that each type may represent a single species, contrary to previous speculations based on morphological data. All merocercoid specimens formed a clade together with Clistobothrium montaukensis. Based on the low degree of divergence, all specimens of this clade are predicted to be congeneric.

Type
Research Article
Copyright
2005 Cambridge University Press

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References

REFERENCES

BAER, J. G. ( 1932). Contribution à l'étude des Cestodes de Cétacés. Revue Suisse de Zoologie 39, 195228.Google Scholar
BALBUENA, J. A. ( 1991). Estudio taxonómico y ecológico de la parasitofauna del calderón común, Globicephala melas (Traill, 1809), en las aguas de Europa. Ph.D. thesis, University of Valencia.
BESTER, M. N. ( 1989). Endoparasites of the subantarctic fur seal Arctocephalus tropicalis from Gough Island. South African Journal of Zoology 24, 363365.CrossRefGoogle Scholar
BRICKLE, P., OLSON, P. D., LITTLEWOOD, D. T. J., BISHOP, A. & ARKHIPKIN, A. I. ( 2001). Parasites of Loligo gahi from waters off the Falkland Islands, with a phylogenetically based identification of their cestode larvae. Canadian Journal of Zoology 79, 22892296.CrossRefGoogle Scholar
CAIRA, J. N., JENSEN, K. & HEALY, C. J. ( 1999). On the phylogenetic relationships among tetraphyllidean, lecanicephalidean and diphyllidean tapeworm genera. Systematic Parasitology 42, 77151.CrossRefGoogle Scholar
CHAMBERS, C. B., CRIBB, T. H. & JONES, M. K. ( 2000). Tetraphyllidean metacestodes of teleosts of the Great Barrier Reef, and the use of in vitro cultivation to identify them. Folia Parasitologica 47, 285292.CrossRefGoogle Scholar
CHERVY, L. ( 2002). The terminology of larval cestodes or metacestodes. Systematic Parasitology 52, 133.CrossRefGoogle Scholar
DAILEY, M. D. ( 1985). Diseases of Mammalia: Cetacea. In Diseases of Marine Animals ( ed. Kinne, O.). Vol. IV, Part 2, pp. 805847. Biologische Anstalt Helgoland, Hamburg, Germany.
DAILEY, M. D. & BROWNELL, R. L. ( 1972). A checklist of marine mammal parasites. In Mammals of the Sea. Biology and Medicine ( ed. Ridgway, S. H.), pp. 528589. C.C. Thomas Publisher, USA.
DAILEY, M. D. & VOGELBEIN, W. ( 1990). Clistobothrium carcharodoni gen. et sp. n. (Cestoda: Tetraphyllidea) from the spiral valve of the great white shark (Carcharodon carcharias). Journal of the Helminthological Society of Washington 57, 108112.Google Scholar
DELYAMURE, S. L. ( 1955). Helminth Fauna of Marine Mammals (Ecology and Phylogeny). Izdatel'stvo Akademii Nauk SSSR, Moscow, Russia. (English translation by M. Raveh, 1968. Israel Program for Scientific Translations, Jerusalem, Israel.)
DOLLFUS, R. P. H. ( 1964). A propos de la récolte, à Banyuls d'un cystique de Cestode chez Tursiops truncatus (Montagu, 1821). Les cystiques des cestodes chez les cétacés et pinnipèdes. Vie Milieu 17, 177204.Google Scholar
EUZET, L. ( 1959). Recherches sur les cestodes tétraphyllides des sélaciens des côtes de France. Ph.D. thesis, University of Montpellier.
EUZET, L. ( 1994). Order Tetraphyllidea Carus, 1863. In Keys to the Cestode Parasites of Vertebrates ( ed. Khalil, L. F., Jones, A. & Bray, R. A.), pp. 149194. Wallingford: CAB International.
FREEMAN, R. S. ( 1973). Ontogeny of cestodes and its bearing on their phylogeny and systematics. Advances in Parasitology 11, 401557.CrossRefGoogle Scholar
GARIPPA, G., SCALA, A. & PAIS, A. ( 1991). Phyllobothrium delphini and Pennella sp. in a dolphin of the species Stenella coeruleoalba. Bollettino della Società Italiana di Patologia Ittica 6, 1924.Google Scholar
GUIART, M. J. ( 1935). Cestodes parasites provenant des campagnes scientifiques du Prince Albert 1er de Monaco. Résultats des Campagnes Scientifiques du Prince de Monaco, Monaco 91, 1105.Google Scholar
HAMILTON, K. A. & BYRAM, J. E. ( 1974). Tapeworm development: the effects of urea on a larval tetraphyllidean. Journal of Parasitology 60, 2028.CrossRefGoogle Scholar
HUELSENBECK, R. & RONQUIST, F. ( 2001). MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755.CrossRefGoogle Scholar
JOHNSTON, T. H. & MAWSON, P. M. ( 1939). Internal parasites of the pigmy sperm whale. Records of the South Australian Museum 6, 263274.Google Scholar
LINTON, E. ( 1905). Notes on cestode cyst, Taenia chamissonii, new species, from a porpoise. Proceedings of the United States National Museum 28, 819823.CrossRefGoogle Scholar
LINTON, E. ( 1922). A new cestode from the maneater and mackerel sharks. Proceedings of the United States National Museum 61, 116.CrossRefGoogle Scholar
MADDISON, D. R. & MADDISON, W. P. ( 2000). MacClade 4: Analysis of Phylogeny and Character Evolution. Version 4.06. Sinauer Associates, Inc., Sunderland, Mass.
MARKOWSKI, S. ( 1955). Cestodes of whales and dolphins from the Discovery Collections. Discovery Reports 27, 377395.Google Scholar
MENDONÇA, M. M. ( 1984). Phyllobothrium delphini (Bosc, 1802) (Cestoda, Tetraphyllidea) from Arctocephalus pusillus (Schreber, 1778) (Carnivora, Otariidae) in captivity. Revista Iberica de Parasitologia 44, 3944.Google Scholar
NYLANDER, J. ( 2002). MrModeltest Version 1.1b. Department of Systematic Zoology, EBC, Uppsala, Sweden.
OLSON, P. D., LITTLEWOOD, D. T. J., BRAY, R. A. & MARIAUX, J. ( 2001). Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Molecular Phylogenetics and Evolution 19, 443467.CrossRefGoogle 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 Scholar
POSADA, D. & CRANDALL, K. A. ( 1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817818.CrossRefGoogle Scholar
RAGA, J. A. ( 1985). Contribución al estudio del parasitismo y demás asociaciones en los cetáceos de la Península Ibérica. Ph.D. thesis, University of Valencia.
RAGA, J. A. ( 1994). Parasitismus bei den Cetacea. In Handbuch der Säugetiere Europas ( ed. Robineau, D., Duguy, R. & Klima, M.). Band 6/I A Meeressäuger, Teil I A: Wale und Delphine 1, pp. 132179. Aula-Verlag Wiesbaden.
REYDA, F. & OLSON, P. D. ( 2003). Cestodes of Peruvian freshwater stingrays. Journal of Parasitology 89, 10181024.CrossRefGoogle Scholar
RUHNKE, T. R. ( 1993). A new species of Clistobothrium (Cestoda: Tetraphyllidea), with an evaluation of the systematic status of the genus. Journal of Parasitology 79, 3743.CrossRefGoogle Scholar
RUHNKE, T. R. ( 1996). Taxonomic resolution of Phyllobothrium van Beneden (Cestoda: Tetraphyllidea) and a description of a new species from the leopard shark Triakis semifasciata. Systematic Parasitology 33, 112.CrossRefGoogle Scholar
SIQUIER, G. F. & LE BAS, A. E. ( 2003). Morphometrical categorization of Phyllobothrium delphini (Cestoidea, Tetraphyllidea) cysts from Fraser's dolphin, Lagenodelphis hosei (Cetacea, Delphinidae). Latin American Journal of Aquatic Mammals 2, 95100.Google Scholar
SKRJABIN, A. S. ( 1964). [Helminth larval forms of marine mammals from Far East seas]. In Morskie Mlekopitayushchie, pp. 311316. Moscow: Nauka [in Russian].
SKRJABIN, A. S. ( 1970). The first finding of larvae of the cestode Monorygma delphini (Tetraphyllidea, Phyllobothriidae) in Antarctic whales. Zoologicheskii Zhurnal 49, 17211722 [in Russian].Google Scholar
SKRJABIN, A. S. ( 1972). Larvae of cestodes of the genus Phyllobothrium Beneden, 1850 (Tetraphyllidea), parasites of whales and other marine animals. Parazitologiya 6, 426434 [in Russian].Google Scholar
SOULIER, L. ( 1993). Contribution à l’étude de la faune parasitaire des cétacés. Ph.D. thesis, Université Claude Bernard de Lyon.
SOUTHWELL, T. & WALKER, A. J. ( 1936). Notes on a larval cestode from a fur seal. Annals of Tropical Medicine and Parasitology 30, 91100.CrossRefGoogle Scholar
SWOFFORD, D. L. ( 2001). Phylogenetic Analysis using Parsimony (*and other Methods). Vers. 4. Sinauer, Sunderland, Massachusetts.
TESTA, J. & DAILEY, M. D. ( 1977). Five new morphotypes of Phyllobothrium delphini (Cestoda: Tetraphyllidea), their relationship to existing morphotypes, and their zoogeography. Bulletin of the Southern California Academy of Sciences 76, 99110.Google Scholar
WALKER, W. A. ( 2001). Geographical variation of the parasite, Phyllobothrium delphini (Cestoda), in Dall's porpoise, Phocoenoides dalli, in the Northern North Pacific, Bering Sea and Sea of Okhotsk. Marine Mammal Science 17, 264275.CrossRefGoogle Scholar
WARDLE, R. A. & McLEOD, J. A. ( 1952). The Zoology of Tapeworms. University of Minnesota Press, Minneapolis.