Skip to main content

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

  • C. AGUSTÍ (a1), F. J. AZNAR (a1), P. D. OLSON (a2), D. T. J. LITTLEWOOD (a2), A. KOSTADINOVA (a1) (a3) and J. A. RAGA (a1)...

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.

Corresponding author
Marine Zoology Unit, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, P.O. Box 22085, 46071 Valencia, Spain. Tel: +34 96 354 36 85. Fax: +34 96 354 37 33. E-mail:
Hide All


BAER, J. G. ( 1932). Contribution à l'étude des Cestodes de Cétacés. Revue Suisse de Zoologie 39, 195228.
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.
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.
CAIRA, J. N., JENSEN, K. & HEALY, C. J. ( 1999). On the phylogenetic relationships among tetraphyllidean, lecanicephalidean and diphyllidean tapeworm genera. Systematic Parasitology 42, 77151.
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.
CHERVY, L. ( 2002). The terminology of larval cestodes or metacestodes. Systematic Parasitology 52, 133.
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.
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.
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.
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.
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.
HAMILTON, K. A. & BYRAM, J. E. ( 1974). Tapeworm development: the effects of urea on a larval tetraphyllidean. Journal of Parasitology 60, 2028.
HUELSENBECK, R. & RONQUIST, F. ( 2001). MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755.
JOHNSTON, T. H. & MAWSON, P. M. ( 1939). Internal parasites of the pigmy sperm whale. Records of the South Australian Museum 6, 263274.
LINTON, E. ( 1905). Notes on cestode cyst, Taenia chamissonii, new species, from a porpoise. Proceedings of the United States National Museum 28, 819823.
LINTON, E. ( 1922). A new cestode from the maneater and mackerel sharks. Proceedings of the United States National Museum 61, 116.
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.
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.
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.
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.
POSADA, D. & CRANDALL, K. A. ( 1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817818.
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.
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.
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.
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.
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].
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].
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.
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.
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.
WARDLE, R. A. & McLEOD, J. A. ( 1952). The Zoology of Tapeworms. University of Minnesota Press, Minneapolis.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 8
Total number of PDF views: 17 *
Loading metrics...

Abstract views

Total abstract views: 119 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 19th January 2018. This data will be updated every 24 hours.