Acta Parasitologica

, Volume 59, Issue 2, pp 316–322 | Cite as

Endohelminth parasites of the leafscale gulper shark, Centrophorus squamosus (Bonnaterre, 1788) (Squaliformes:Centrophoridae) off Madeira Archipelago

  • Graça Costa
  • Tomás Chada
  • Egberto Melo-Moreira
  • Serena Cavallero
  • Stefano D’Amelio
Original Paper


The endohelminth parasite fauna of a deep water shark, the leafscale gulper shark, Centrophorus squamosus, examined from Madeiran waters, from September 2009 to January 2010, consisted of larval and juvenile cestodes of two orders, namely Trypanorhyncha and Tetraphyllidea, and L3 stages of Anisakis spp. Infection with Anisakis spp. could be due to the shark’s opportunistic feeding on squids and black-scabbard fish, Aphanopus carbo, which is heavily parasitized by Anisakis spp. in Madeira waters. The occurrence of larval and juvenile cestodes only, in this shark, suggests that the leafscale gulper shark features as a paratenic or a dead-end host for the parasites.


Tetraphyllidea Trypanorhyncha Anisakidae Centrophorus squamosus Madeira Island 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Bañon R., Piñeiro C., Casas J.M. 2006. Biological aspects of deepwater sharks Centroscymnus coelolepis and Centrophorus squamosus in Galician waters (northwestern Spain). Journal of the Marine Biological Association UK, 86, 843–846. DOI: 10.1017/S0025315406013774.CrossRefGoogle Scholar
  2. Berland B. 1961. Nematodes from some Norwegian marine fishes. Sarsia, 2, 1–50.Google Scholar
  3. Berman R., Brooks D.R. 1994. Escherbothrium molinae n. gen. et n. sp. (Eucestoda: Tetraphyllidea: Triloculariidae) in Urotrygon chilensis (Chondrichthyes: Myliobatiformes: Urolophidae) from the Gulf of Nicoya, Costa Rica. Journal of Parasitology, 80, 775–780. DOI: 10.2307/3283257.PubMedCrossRefGoogle Scholar
  4. Beveridge I., Justine J.L. 2006. Gilquiniid cestodes (Trypanorhyncha) from elasmobranch fishes off New Caledonia with descriptions of two new genera and a new species. Systematic Parasitology, 65, 235–249. DOI: 10.1007/s11230-006-9052-8.PubMedCrossRefGoogle Scholar
  5. Beveridge I., Campbell R.A. 2013. A new species of Grillotia Guiart, 1927 (Cestoda: Trypanorhyncha) with redescriptions of congeners and new synonyms. Systematic Parasitology, 85, 99–116. DOI: 10.1007/s11230-013-9416-9.PubMedCrossRefGoogle Scholar
  6. Bush A.O., Lafferty K.D., Lotz J.M., Shostak A.W. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83, 575–583. DOI: 10.2307/328 4227.PubMedCrossRefGoogle Scholar
  7. Caira J.N. 1990. Metazoan parasites as indicators of elasmobranch biology. NOAA Technical Report, 90, 71–96.Google Scholar
  8. Campbell R.A. 1990. Deepwater parasites. Annales de Parasitologie Humaine et Comparée, 65, 65–68.PubMedGoogle Scholar
  9. Cavallero S., Nadler S.A., Paggi L., Barros N.B., D’Amelio S. 2011. Molecular characterization and phylogeny of anisakid nematodes from cetaceans from southeastern Atlantic coasts of USA, Gulf of Mexico, and Caribbean Sea. Parasitology Research, 108, 781–792. DOI: 10.1017/s00436-010-2226-y.PubMedCrossRefGoogle Scholar
  10. Clarke M.W., Connolly P.L., Bracken J.J. 2001. Aspects of reproduction of the deep-water sharks Centroscymnus coelolepis and Centrophorus squamosus from west of Ireland and Scotland. Journal of the Marine Biological Association UK, 81, 1019–1029. DOI: 10.1017/S0025315401005008.CrossRefGoogle Scholar
  11. Compagno L., Dando M., Fowler S. 2005. A Field Guide to the Sharks of the World. Harper Collins Publishers Ltd, London, UK, 368 pp.Google Scholar
  12. Compagno L.J.V. 1984. Vol. 4. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Part 1-Hexanchiformes to Lamniformes. FAO Fisheries Synopsis 125, FAO, Rome, Italy, 1–249.Google Scholar
  13. Cortés E. 1999. Standardized diet compositions and trophic levels of sharks. ICES Journal of Marine Science, 56, 707–717. DOI: 10.1006/jmsc.1999.0489.CrossRefGoogle Scholar
  14. Costa G., Pontes T., Mattiucci S., D’Amelio S. 2003. The occurrence and infection dynamics of Anisakis larvae in the black-scabbard fish, Aphanopus carbo, chub mackerel, Scomber japonicus and oceanic horse mackerel, Trachurus picturatus from Madeira, Portugal. Journal of Helminthology, 77, 163–166. DOI: 10.1079/JOH2002156.PubMedCrossRefGoogle Scholar
  15. D’Amelio S., Mathiopoulos K.D., Santos C.P., Pugachev O.N., Webb S.C., Picanço M., Paggi L. 2000. Genetic markers in ribosomal DNA for the identification of members of the genus Anisakis (Nematoda: Ascaridoidea) defined by polymerase chain reaction-based restriction fragment length polymorphism. International Journal for Parasitology, 30, 223–226. DOI: 10.1016/S0020-7519(99)00178-2.PubMedCrossRefGoogle Scholar
  16. Euzet L. 1959. Les Cestodes Tetraphyllides. Recueil des travaux des laboratoires de Botanique, Géologie et Zoologie de la Faculté des Sciences de L’ Université de Montpellier, Série Zoologie (Fascicule III), Montpellier, 296 pp.Google Scholar
  17. Euzet L. 1994. Order Tetraphyllidea Carus, 1863. In: (Eds. L.F. Khalil, A. Jones and R.A. Bray) Keys to the Cestoda Parasites of Vertebrates. CAB International, Oxon, UK, 149–194.Google Scholar
  18. Figueiredo I., Moura T., Neves A., Gordo L.S. 2008. Reproductive strategy of leafscale gulper shark Centrophorus squamosus and the Portuguese dogfish Centroscymnus coelolepis on the Portuguese continental slope. Journal of Fish Biology, 73, 206–225. DOI: 10.1111/j.1095-8649.2008.01927.x.CrossRefGoogle Scholar
  19. Freitas I.C.L. 1998. Contribuição para o conhecimento da ecologia alimentar do peixe espada preto, Aphanopus carbo Lowe 1839 (Pisces: Trichiuridae) no Arquipélago da Madeira. Diploma thesis, University of Madeira, Portugal (in Portuguese).Google Scholar
  20. Freitas M.N.B. 1998. Contribuição para o conhecimento da ecologia trófica da xara branca, Centrophorus squamosus (Bonnaterre 1788) (Chondrichthyes: Squalidae) no Arquipelágo da Madeira. Diploma thesis, University of Madeira, Portugal. (in Portuguese).Google Scholar
  21. Froese R., Pauly D. 2011. Fishbase. World Wide Web electronic publication. Accessed on 31st October 2013., version 08/2011.Google Scholar
  22. Girard M., Du Buit M.H. 1999. Reproductive biology of two deepwater sharks from the British Isles, Centroscymnus coelolepis and Centrophorus squamosus. Journal of the Marine Biological Association UK, 79, 923–931. DOI:10.1017/S0025315 49800109X.CrossRefGoogle Scholar
  23. Guallart J., Serena F., Mancusi C., Casper B.M., Burgess G.H., Ebert D.A., Clarke M., Stenberg C. 2006. Centrophorus granulosus. In: IUCN 2011. IUCN Red list of threatened species. Version 2011.2 ( Accessed on 31st October 2013.Google Scholar
  24. Klimpel S., Seehagen A., Palm H.W. 2003. Metazoan parasites and food composition of juvenile Etmopterus spinax (L., 1758) (Dalatiidae, Squaliformes). Parasitology Research, 89, 245–251. DOI: 10.1007/s00436-002-0741-1.PubMedGoogle Scholar
  25. Klimpel S., Seehagen A., Palm H.W., Rosenthal H. 2001. Deep-water metazoan fish parasites of the world. Logos, Berlin, Germany, 316 pp.Google Scholar
  26. Mattiucci S., Nascetti G. 2008. Chapter 2: Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host-parasite co-evolutionary processes. Advances of Parasitology, 66, 47–148. DOI: 10.1016/S0065-308X(08)00202-9.CrossRefGoogle Scholar
  27. Mattiucci S., Nascetti G., Cianchi R., Paggi L., Arduino P., Margolis L., Brattey J., Webb S., D’Amelio S., Orecchia P., Bullini L. 1997. Genetic and ecological data on the Anisakis simplex complex with evidence for a new species (Nematoda, Ascaridoidea, Anisakidae). Journal of Parasitology, 86, 401–416. DOI: 10.2307/3284402.CrossRefGoogle Scholar
  28. McCullough J.S., Fairweather I. 1983. A SEM study of the cestodes Trilocularia acanthiaevulgaris, Phyllobothrium squali and Gilquinia squali from the spiny dogfish. Zeitschrift Parasitenkunde, 69, 655–665. DOI: 10.1007/BF00926675.CrossRefGoogle Scholar
  29. McCullough J.S., Fairweather I. 1984. A comparative study of Trilocularia acanthiaevulgaris Olsson 1867 (Cestoda, Tetraphyllidea) from the stomach and spiral valve of the spiny dogfish. Zeitschrift Parasitenkunde, 70, 797–807. DOI: 10.1007/BF 00927132.CrossRefGoogle Scholar
  30. McCullough J.S., Fairweather I., Montgomery W.I. 1986. The seasonal occurrence of Trilocularia acanthiaevulgaris (Cestoda: Tetraphyllidea) from the spiny dogfish in the Irish Sea. Parasitology, 93, 153–162. DOI: 10.1017/S0031182000049908.PubMedCrossRefGoogle Scholar
  31. Moura T., Silva M.C., Figueiredo I., Neves A., Dúran Muñoz P., Coelho M.M., Gordo L. 2008. Molecular barcoding of north-east Atlantic deep-water sharks: species identification and application to fisheries management and conservation. Marine and Freshwater Research, 59, 214–223. DOI: 10.1071/MF07192.CrossRefGoogle Scholar
  32. Palm H.W. 2004. The Trypanorhyncha Diesing, 1863. PKSPL-IPB Press, Bogor, Indonesia, 710 pp.Google Scholar
  33. Palm H.W., Schröber P. 2001. Cestode parasites from the elasmobranches Heptranchias perlo and Deania from the Great Meteor Bank, Central East Atlantic. Aquatic Living Resources, 14, 137–144. DOI: 10.1016/S0990-7440(01)01107-X.CrossRefGoogle Scholar
  34. Pontes T., D’Amelio S., Costa G., Paggi L. 2005. Molecular characterization of larval anisakid nematodes from marine fishes of Madeira by a PCR based approach with evidence for a new species. Journal of Parasitology, 90, 1430–1434. DOI: 10.1645/GE-565R1.1.CrossRefGoogle Scholar
  35. Tazerouti F., Euzet L., Kechemir-Issad N. 2007. Redescription de trois espèces de Calyptrobothrium Monticelli, 1893 (Tetraphyllidea: Phyllobothriidae) parasites de Torpedo marmorata et T. nobiliana (Elasmobranchii: Torpedinidae). Remarques sur leur spécificité parasitaire et sur la position taxonomique des espèces auparavant attribuées à C. riggii Monticelli, 1893. Systematic Parasitology, 67, 175–185. DOI:10.1007/s11230-006-9088-9.PubMedCrossRefGoogle Scholar
  36. White W.T. 2003. Centrophorus squamosus. In: IUCN 2011. IUCN Red list of threatned species. Version 2011.2 ( Accessed on 31st October 2013.Google Scholar
  37. White W.T., Dharmadi. 2010. Aspects of maturation and reproduction in hexanchiform and squaliform sharks. Journal of Fish Biology, 76, 1362–1378. DOI: 10.1111/j.1095-8649.2010.02 560.x.PubMedCrossRefGoogle Scholar
  38. Zhu X., D’Amelio S., Paggi L., Gasser R.B. 2000. Assessing sequence variation in the internal transcribed spacers of the ribosomal DNA within and among members of the Contracaecum osculatum complex (Nematoda: Ascaridoidea: Anisakidae). Parasitology Research, 86, 677–683. DOI: 10.1007/PL00008551.PubMedCrossRefGoogle Scholar

Copyright information

© Versita Warsaw and Springer-Verlag Wien 2014

Authors and Affiliations

  • Graça Costa
    • 1
    • 2
  • Tomás Chada
    • 1
  • Egberto Melo-Moreira
    • 1
  • Serena Cavallero
    • 3
  • Stefano D’Amelio
    • 3
  1. 1.Estação de Biologia Marinha do FunchalUniversidade da Madeira, Promenade Orla Marítima do FunchalFunchalPortugal
  2. 2.ISOPlexisUniversidade da MadeiraFunchalPortugal
  3. 3.Department of Public Health SciencesUniversity of Rome La SapienzaPiazzale Aldo MoroItaly

Personalised recommendations