Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-28T17:01:53.409Z Has data issue: false hasContentIssue false
  • English
  • Français

Parasites of Scyliorhinus canicula (Linnaeus, 1758) in the north-eastern Aegean Sea

Published online by Cambridge University Press:  11 September 2017

Vasileios Bakopoulos ,
Euaggelia Tsepa ,
Anastasia Diakou ,
Giorgos Kokkoris ,
Markos Nikolaos Kolygas  and
Foteini Athanassopoulou
Vasileios Bakopoulos*
Affiliation:
Department of Marine Sciences, School of The Environment, University of The Aegean, University Hill, Mytilene 81100, Greece
Euaggelia Tsepa
Affiliation:
Department of Marine Sciences, School of The Environment, University of The Aegean, University Hill, Mytilene 81100, Greece
Anastasia Diakou
Affiliation:
School of Veterinary Medicine, Faculty of Health Sciences, Aristotle University of Thessaloniki, Thessaloniki 54124, Greece
Giorgos Kokkoris
Affiliation:
Department of Marine Sciences, School of The Environment, University of The Aegean, University Hill, Mytilene 81100, Greece
Markos Nikolaos Kolygas
Affiliation:
Faculty of Veterinary Medicine, University of Thessaly, Karditsa, Greece
Foteini Athanassopoulou
Affiliation:
Faculty of Veterinary Medicine, University of Thessaly, Karditsa, Greece
*
Correspondence should be addressed to: V. Bakopoulos Laboratory of Ichthyology, Aquaculture & Aquatic Animals Diseases, Department of Marine Sciences, University of The Aegean, University Hill, Mytilene 81100, Lesvos, Greece email: bakopoulos@marine.aegean.gr
Get access Rights & Permissions [Opens in a new window]

Abstract

The parasitic fauna of the small-spotted catshark, Scyliorhinus canicula in the north-eastern Aegean Sea was investigated. Twenty-one out of the 52 (prevalence 40.4%) specimens collected were found infected with parasites; an arthropod and two nematode genera. Seven specimens (prevalence 13.5%) were infected by a Neoalbionella sp. copepod. Ten and 14 specimens were infected by the nematodes Proleptus obtusus (prevalence 19.2%) and Anisakis sp. (prevalence 26.9%), respectively. Female S. canicula specimens were significantly more heavily infected during autumn and when the whole sampling period is considered. Nematode infection was significantly related to season, becoming progressively heavier from spring to autumn. No correlation was found between TL of specimens and number of parasites for males or females, irrespective of gender. The present study provided a first record of Neoalbionella sp., P. obtusus and Anisakis sp. infections of S. canicula in the north-eastern Mediterranean. The lower prevalence of Proleptus obtusus and the higher prevalence of Anisakis sp. infection recorded in this study may be due to prey availability and parasite populations in this locality.

Keywords

Scyliorhinus caniculaNeoalbionella sp.Proleptus obtususAnisakis sp.small-spotted catsharkparasites
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Special Issue 8: Special Section: European Marine Biology Symposium Papers 2018 , December 2018 , pp. 2133 - 2143
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abollo, E., Gestal, C. and Pascual, S. (2001) Anisakis infestation in marine fish and cephalopods from Galicia waters: an update perspective. Parasitology Research 87, 492–499.Google Scholar
Armstrong, M.J. (1982) The predator-prey relationships of Irish Sea poor-cod (Trisopterus minutus L.), pouting (Trisopterus luscus L), and cod (Gadus morhua L.). ICES Journal of Marine Science 40, 135–152.Google Scholar
Athanassopoulou, F. (1990) A study of the Myxosporean infections of R. rutilus L. with special reference to Myxidium rhodei Leger, 1905 in the renal tissue. PhD thesis. University of Stirling, Stirling, UK.Google Scholar
Banon, R., Villegas-Ríos, D., Serrano, A., Mucientes, G. and Arronte, J.C. (2010) Marine fishes from Galicia (NW Spain): an updated checklist. Zootaxa 2667, 1–27.Google Scholar
Benz, G.W. (1991a) Redescription of Lernaeopoda oviformis Shiino, 1956 (Copepoda: Lernaeopodidae), a parasite of the shortspine spurdog (Squalus mitsukurii Jordan & Snyder, 1903), and hitherto covert member of Albionella Kabata, 1979. Canadian Journal of Zoology 69, 567–570.Google Scholar
Benz, G.W. (1991b) Description of some larval stages and augmented description of adult stages of Albionella etmopteri (Copepoda: Lernaeopodidae), a parasite of deep-water lanternsharks (Etmopterus: Squalidae). Journal of Parasitology 77, 666–674.Google Scholar
Benz, G.W. and Izawa, K. (1990) Albionella kabatai sp. nov. (Lernaeopodidae: Siphonostomatoida), a copepod parasite of the spatula snout cat shark (Apristurus platyrhynchus (Tanaka, 1909)) from the Sea of Kumano. Canadian Journal of Zoology 68, 2645–2648.Google Scholar
Berland, B. (1961) Nematodes from some Norwegian marine fishes. Sarsia 2, 1–50.Google Scholar
Bilecenoglu, M., Taskavak, E., Mater, S. and Kaya, M. (2002) Checklist of the marine fishes of Turkey. Zootaxa 113, 1–194.Google Scholar
Boxshall, G.A. (1998) Host specificity in copepod parasites of deep-sea fishes. Journal of Marine Systems 15, 215–223.Google Scholar
Bray, R.A. (2001) Cestoda. In Costello, M.J., Emblow, C. and White, R.J. (eds) European register of marine species: a check-list of the marine species in Europe and a bibliography of guides to their identification. Collection Patrimoines Naturels 50. Paris: Muséum national d'Histoire naturelle, pp. 146–149.Google Scholar
Bray, R.A. and Moore, A.B.M. (2000) The first record of the elasmobranch parasite Diphterostomum betencourti (Monticelli, 1893) (Digenea, Zoogonidae) in the coastal waters of southern England. Acta Parasitologica 45, 299–302.Google Scholar
Brunel, P., Bosse, L. and Lamarche, G. (1998) Catalogue of the marine invertebrates of the estuary and Gulf of St. Lawrence. Canadian Special Publication of Fisheries and Aquatic Sciences 126, 405 pp.Google Scholar
Bush, A.O., Lafferty, K.D., Lotz, J.M. and Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.Google Scholar
Butler, P.J. and Taylor, E.W. (1975) The effect of progressive hypoxia on respiration in the dogfish (Scyliorhinus canicula) at different seasonal temperatures. Journal of Experimental Biology 63, 117–130.Google Scholar
Cannon, L.R. (1977) Some larval ascaridoids from south-eastern Queensland marine fishes. International Journal of Parasitology 7, 233–243.Google Scholar
Casadevall, M., Martinez, N. and King, P. (2010) The lesser-spotted dogfish (Scyliorhinus canicula): parasites and scavenger habits. Rapport Commission International de Mer Méditerranee 39, 470.Google Scholar
Compagno, L.J.V. (1984) FAO Species Catalogue. Vol. 4. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Part 2 – Carcharhiniformes. FAO Fisheries Synopsis 125, 251–655.Google Scholar
Dujardin, F. (1845) Histoire naturelle des helminthes ou vers intestinaux. Paris: Librairie Encyclopédique de Roret, pp. xvi +654 +15.Google Scholar
Ellis, J.R., Cruz-Martinez, A., Rackham, B.D. and Rodgers, S.I. (2005) The distribution of Chondrichthyan fishes around the British Isles and implications for conservation. Journal of Northwestern Atlantic Fisheries Science 35, 195–213.Google Scholar
Ellis, J.R., Pawson, M.G. and Shackley, S.E. (1996) The comparative feeding ecology of six species of shark and four species of ray (Elasmobranchii) in the north-east Atlantic. Journal of the Marine Biological Association of the United Kingdom 76, 89–106.Google Scholar
Ellis, J.R. and Shackley, S.E. (1997) The reproductive biology of Scyliorhinus canicula in the Bristol Channel, U.K. Journal of Fish Biology 51, 361–372.Google Scholar
FAO (2016) Fishery and aquaculture statistics. FAO 2016 Yearbook. Rome: FAO, 619 pp.Google Scholar
Gibson, R.N. and Ezzi, I.A. (1987) Feeding relationships of a demersal fish assemblage on the west coast of Scotland. Journal of Fish Biology 31, 55–69.Google Scholar
Gracan, R., Culinovic, M., Mladineo, I., Lackovic, G. and Lazar, B. (2016) Trophic ecology shapes gastrointestinal helminth communities of two sympatric mesopredatory sharks in the Adriatic Sea. Journal of Zoology 299, 172–182.Google Scholar
Hartwich, G. (1974) Keys to genera of the Ascaridoidea. In Anderson, R.C., Chabaud, A.G. and Wilmott, S. (eds) Commonwealth Institute of Helminthology keys to the nematode parasites of vertebrates. Farnham Royal: Commonwealth Agricultural Bureaux, pp. 1–15.Google Scholar
Henderson, A.C. and Dunne, J.J. (1998) The metazoan parasites of the lesser-spotted dogfish Scyliorhinus canicula (L.) from the Galway Bay area. Irish Naturalists Journal 26, 104–107.Google Scholar
Henderson, A.C. and Dunne, J.J. (2001) The distribution of the microbothriid shark parasite Leptocotyle minor on its host, the lesser-spotted dogfish Scyliorhinus canicula. Biology and Environment: Proceedings of the Royal Irish Academy 101B, 251–253.Google Scholar
Heupel, M.R. and Bennett, M.B. (1998) Infection of the epaulette shark, Hemiscyllium ocellatum (Bonnaterre), by the nematode parasite Proleptus australis Bayliss (Spirurida: Physalopteridae). Journal of Fish Diseases 21, 407–413.Google Scholar
IUCN (2012) IUCN red list of threatened species. Version 2012.1.Google Scholar
Kabata, Z. (1979) Parasitic copepoda of British fishes. London: Ray Society, pp. 468.Google Scholar
Kabata, Z. (1986) Redescription of and comments on four little known Lernaeopodidae (Crustacea: Copepoda). Canadian Journal of Zoology 64, 1852–1859.Google Scholar
Kearn, G.C., Evans-Gowing, R. and Rees, J. (2001) An ultrastructural study of the haptor of the microbothriid monogenean Leptocotyle minor from the skin of the dogfish Scyliorhinus canicula (Scyliorhinidae). Acta Parasitologica 46, 254–260.Google Scholar
Labropoulou, M. and Papaconstantinou, C. (2000) Community structure of deep-sea demersal fish in the North Aegean Sea (northeastern Mediterranean). Hydrobiologia 440, 281–296.Google Scholar
Leigh-Sharpe, W.H. (1918) Lernaeopoda globosa n. sp., a parasitic copepod of Scyllium canicula. Part I. Parasitology Cambridge 11, 29–34.Google Scholar
Llewellyn, J., Green, J.E. and Kearn, G.C. (1984) A check-list of monogenean (platyhelminth) parasites of Plymouth hosts. Journal of the Marine Biological Association of the United Kingdom 64, 881–887.Google Scholar
Lloret, J., Faliex, E., Shulman, G.E., Raga, J.-A., Sasal, P., Munoz, M., Casadevall, M., Ahuir-Baraja, A.E., Montero, F.E., Repulles-Albelda, A., Cardinale, M., Ratz, H.-J., Vila, S. and Ferrer, D. (2012) Fish health and fisheries, implications for stock assessment and management: the Mediterranean example. Reviews in Fisheries Science 20, 165–180.Google Scholar
Lyle, J.M. (1983) Food and feeding habits of the lesser spotted dogfish, Scyliorhinus canicula (L.) in Isle of Man waters. Journal of Fisheries Biology 23, 139–148.Google Scholar
Marcogliese, D.J. (2004) Parasites: small players with crucial roles in the ecological theater. Ecosystem Health 1, 151–164.Google Scholar
Marcogliese, D.J. and Cone, D.K. (1997) Food webs: a plea for parasites. Trends in Ecology and Evolution 12, 320–325.Google Scholar
Martinho, F., Sa, C., Falcao, J., Cabral, H.N. and Pardal, M.A. (2012) Comparative feeding ecology of two elasmobranch species, Squalus blainville and Scyliorhinus canicula, off the coast of Portugal. Fishery Bulletin 110, 71–84.Google Scholar
Mattiucci, S., Abaunza, P., Ramadori, L. and Nascetti, G. (2004) Genetic identification of Anisakis larvae in European hake from Atlantic and Mediterranean waters for stock recognition. Journal of Fish Biology 65, 495–510.Google Scholar
Mattiucci, S., Farina, V., Campbell, N., MacKenzie, K., Ramos, P., Pinto, A.L., Abaunza, P. and Nascetti, G. (2008) Anisakis spp. larvae (Nematoda: Anisakidae) from Atlantic horse mackerel: their genetic identification and use as biological tags for host stock characterization. Fisheries Research 89, 146–151.Google Scholar
McClelland, G. and Martell, D.J. (2001) Surveys of larval sealworm (Pseudoterranova decipiens) infection in various fish species sampled from Nova Scotian waters between 1988 and 1996, with an assessment of examination procedures. In Desportes, G. and McClelland, G. (eds) Sealworms in the North Atlantic: ecology and population dynamics. Tromso: North Atlantic Marine Mammal Commission, pp. 57–76.Google Scholar
McClelland, G., Misra, R.K. and Martell, D.J. (1990) Larval anisakis nematodes in various fish species from Sable Island Bank and vicinity. In Bowen, B.R. (ed.) Population biology of silkworm (Pseudoterranova decipiens) in relation to its intermediate and seal hosts. Canadian Bulletin of Fisheries and Aquatic Science 222, 83–118.Google Scholar
Mladineo, I. and Poljak, V. (2014) Ecology and genetic structure of zoonotic Anisakis spp. from Adriatic commercial fish species. Applied and Environmental Microbiology 80, 1281–1290.Google Scholar
Moore, A.B.M. (2001) Metazoan parasites of the lesser-spotted dogfish Scyliorhinus canicula and their potential as stock discrimination tools. Journal of the Marine Biological Association of the United Kingdom 81, 1009–1013.Google Scholar
Moravec, F. (2007) Some aspects of the taxonomy and biology of adult spirurine nematodes parasitic in fishes: a review. Folia Parasitologica 54, 239–257.Google Scholar
Moravec, F., Van As, J.G. and Dykova, I. (2002) Proleptus obtusus Dujardin, 1845 (Nematoda: Physalopteridae) from the puffadder shyshark Haploblepharus edwardsii (Scyliorhinidae) from off South Africa. Systematic Parasitology 53, 169–173.Google Scholar
Muus, B.J. and Nielsen, J.G. (1999) Die meeresfische Europas in Nordsee, Ostsee und Atlantik. Stuttgart: Kosmos-Naturfuhrer.Google Scholar
Mytilineou, C., Politou, C.-Y., Papaconstantinou, C., Kavadas, S., D'Onghia, G. and Sion, L. (2005) Deep-water fish fauna in the Eastern Ionian Sea. Belgian Journal of Zoology 135, 229–233.Google Scholar
Olaso, I., Velasco, F. and Pérez, N. (1998) Importance of discarded blue whiting (Micromessistius poutassou) in the diet of lesser spotted dogfish (Scyliorhinus canicula) in the Cantabrian Sea. ICES Journal of Marine Science 55, 331–341.Google Scholar
Olaso, I., Velasco, F., Sanchez, F., Serrano, A., Rodriguez-Cabello, C. and Cendrero, O. (2005) Trophic relations of lesser-spotted catshark (Scyliorhinus canicula) and blackmouth catshark (Galeus melastomus) in the Cantabrian Sea. Journal of Northwest Atlantic Fisheries Science 35, 481–494.Google Scholar
Özdikmen, H. (2008) Nomenclatural changes for nine crustacean genera (Crustacea: Copepoda). Munis Entomology and Zoology 3, 265–274.Google Scholar
Palm, H.W. (2004) The Trypanorhyncha Diesing, 1863. Bogor: PKSPL-IPB Press. ISBN 979-9336-39-2.Google Scholar
Perari, M. (2010) Data on the feeding habits of Scyliorhinus canicula (Linnaeus, 1758) in the North-eastern Aegean Sea. Graduate thesis, Department of Marine Sciences, School of The Environment, University of The Aegean, Lesvos, Greece.Google Scholar
Pollerspöck, J. and Straube, N. (2015) Bibliography database of living/fossil sharks, rays and chimaeras (Chondrichthyes: Elasmobranchii, Holocephali) -Host-Parasites List/Parasite-Hosts List-, www.sharkreferences.com. doi: 10.13140/RG.2.1.3636.6887.Google Scholar
Pozio, E. (2013) Integrating animal health surveillance and food safety: the example of Anisakis. Reviews of Science & Technology, Office International de Epizooties 32, 487–496.Google Scholar
Raibaut, A., Combes, C. and Benoit, F. (1998) Analysis of the parasitic copepod species richness among Mediterranean fish. Journal of Marine Systems 15, 185–206.Google Scholar
Rees, G. (1959) Ditrachybothridium macrocephalum gen. nov., sp. nov., a cestode from some elasmobranch fishes. Parasitology 49, 191–209.Google Scholar
Reiczigel, J. and Rózsa, L. (2005) Quantitative parasitology 3.0. Software. Budapest: Distributed by the Authors.Google Scholar
Rello, F.J., Adroher, F.J., Benitez, R. and Valero, A. (2009) The fishing area as a possible indicator of the infection by anisakids in anchovies (Engraulis encrasicolus) from southwestern Europe. International Journal of Food Microbiology 129, 277–281.Google Scholar
Roberts, R.J. (1989) Fish pathology. 2nd edition. London: Baillière Tindall.Google Scholar
Rodríguez, S.M., Luque, J.L. and Nascimento, M.G. (2010) A parasitic copepod, Neoalbionella sp. (Lernaeopodidae), on the southern lanternshark Etmopterus granulosus (Etmopteridae) off Juan Fernández Archipelago, Chile. Revista de Biología Marina y Oceanografía 45, 359–363.Google Scholar
Rubec, L.A. and Hogans, W.E. (1988) Albionella fabricii n. sp. (Copepoda: Lernaeopodidae) from the gills of Centroscyllium fabricii from the Northwest Atlantic. Systematic Parasitology 11, 219–225.Google Scholar
Sanmartín Durán, M.L., Quinteiro, P. and Ubeira, F.M. (1989) Nematode parasites of commercially important fish in NW Spain. Diseases of Aquatic Organisms 7, 75–77.Google Scholar
Santic, M., Rada, B. and Pallaoro, A. (2012) Feeding habits of small-spotted catshark (Scyliorhinus canicula Linnaeus, 1758) from the eastern central Adriatic Sea. Marine Biology Research 11, 1003–1011.Google Scholar
Silva, C., Verissimo, A., Cardoso, P., Cable, J. and Xavier, R. (2017) Infection of the lesser spotted dogfish with Proleptus obtusus Dujardin, 1845 (Nematoda: Spirurida) reflects ontogenetic feeding behavior and seasonal differences in prey availability. Acta Parasitologica 62, 471–476. doi: 10.1515/ap-2017-00.Google Scholar
Sims, D.W., Nash, J.P. and Morritt, D. (2001) Movements and activity of male and female dogfish in a tidal sea lough: alternative behavioural strategies and apparent sexual segregation. Marine Biology 139, 1165–1175.Google Scholar
Thollot, P. (1996) Les poissons de mangrove du lagon sud-ouest de Nouvelle-Caledonie. Paris: ORSTOM Editions.Google Scholar
Tyler, G.A. (2006) Tapeworms of elasmobranchs (Part II). A monograph on the Diphyllidea (Platyhelminthes, Cestoda). Bulletin of the University of Nebraska State Museum 20, 1–142.Google Scholar
Valls, M., Quetglas, A., Ordines, F. and Moranta, J. (2011) Feeding ecology of demersal elasmobranchs from the shelf and slope off the Balearic Sea (western Mediterranean). Scientia Marina 75, 633–639.Google Scholar
Williams, H. and Jones, A. (1994) Parasitic worms of fish. London: Taylor & Francis.Google Scholar
WoRMS (2017) Available at: http://www.marinespecies.org/aphia.php?p=taxdetails&id=105814 (accessed January 2017).Google Scholar
Yeld, E.M. (2009) Parasite assemblages of three endemic catshark species from the west and south coasts of South Africa. PhD thesis. University of Cape Town, Cape Town, South Africa.Google Scholar