Hostname: page-component-77c89778f8-gq7q9 Total loading time: 0 Render date: 2024-07-22T05:51:24.202Z Has data issue: false hasContentIssue false
  • English
  • Français

Seasonal development and pathological changes associated with the parasitic nematode Philometroides sanguineus in wild crucian carp Carassius carassius (L.) in England

Published online by Cambridge University Press:  05 August 2011

C.F. Williams ,
F. Moravec ,
J.F. Turnbull  and
H.W. Ferguson
C.F. Williams*
Affiliation:
Environment Agency, Bromholme Lane, Brampton, CambridgeshirePE28 4NE, England, UK
F. Moravec
Affiliation:
Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, České Budějovice, Czech Republic
J.F. Turnbull
Affiliation:
Institute of Aquaculture, University of Stirling, StirlingFK9 4LA, Scotland, UK
H.W. Ferguson
Affiliation:
Marine Medicine Programme, School of Veterinary Medicine, St George's University, Grenada, West Indies
*
*Fax: +44 (0)1480 433873E-mail: chris.williams@environment-agency.gov.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

Pathological changes associated with the parasitic nematode Philometroides sanguineus (Rudolphi, 1819) are described for the first time from observations of infections in wild crucian carp Carassius carassius (L.) in England. The damage caused by P. sanguineus was influenced strongly by host size, parasite development and the seasonal migrations of female nematodes within host tissues. Male and unfertilized female nematodes located on the swim-bladder wall caused only minor, localized changes. In contrast, the migration of gravid female nematodes into the fins during autumn provoked an acute inflammatory response comprising neutrophils, eosinophils and lymphocytes. This was accompanied by fin distortion, swelling of the dorsal and caudal tissues, degenerative changes and localized oedema. The encapsulation of female nematodes in connective tissue throughout winter limited additional tissue damage. The emergence of gravid nematodes from the fins in spring to facilitate larval dispersal caused necrosis, hyperplasia and loss of skin integrity. This activity was again accompanied by acute inflammatory reactions. Pathological changes were more severe in crucian carp measuring less than 60 mm in length, with no signs of debilitation in larger fish. These observations suggest that any impact of P. sanguineus is strictly seasonal and may be limited to fry. Lesions caused by this parasite, only recently recorded in Britain, may represent an additional pressure upon wild crucian carp populations already threatened by hybridization, competition and habitat loss.

Type
Research Papers
Information
Journal of Helminthology , Volume 86 , Issue 3 , September 2012 , pp. 329 - 338
Copyright
Copyright © Cambridge University Press 2011

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

Anderson, R.C. (2000) Nematode parasites of vertebrates. Their development and transmission. 2nd edn. 650 pp. Wallingford, CABI Publishing.CrossRefGoogle Scholar
Bauer, O.N., Musselius, V.A. & Strelkov Yu, A. (1969) Diseases of pond fishes. 220 pp. Moscow, Kolos (in Russian; English translation: Israel Program for Scientific Translations, Jerusalem).Google Scholar
Blanc, G. (1997) Introduction of pathogens in European aquatic ecosystems: attempt of evaluation and realities. Bulletin Français de la Pêche et de la Pisciculture 344-345, 37–56.Google Scholar
Bolton, P., Wheeler, A. & Wellby, I.N. (1998) The future of the Crucian carp. IFM 29th annual study course, Homerton College, Cambridge.Google Scholar
Cakay, E. (1957) Nalez Philometroides sanguinaea (Rudolphi, 1819) na Slovensku. Biologia, Bratislava 12, 909–914.Google Scholar
Cheung, P.J., Nigrelli, R.F. & Ruggieri, G.D. (1984) Philometra saltatrix infecting the heart of 0-class bluefish Pomatomus saltatrix (L.) from the New York coast.Abstract Joint Workshop, Fish Health Section, AFS and Midwest Fish Disease Group, Little Rock, Arkansas.Google Scholar
Choudhury, A. & Cole, R.A. (2008) Phylum Nematoda. pp. 1063–1113in Eiras, J.C., Segner, H., Wahli, T. & Kapoor, B.G. (Eds) Fish disease. Enfield, USA, Science Publishers.Google Scholar
Chubb, J.C. (1980) Seasonal occurrence of helminths in freshwater fishes. Part IV Adult Cestoda, Nematoda and Acanthocephala. Advances in Parasitology 20, 1–293.Google Scholar
Copp, G.H., Warrington, S. & Wesley, K.J. (2008) Management of an ornamental pond as a conservation site for a threatened native fish species, crucian carp Carassius carassius. Hydrobiologia 597, 149–155.CrossRefGoogle Scholar
Crichton, V.F.J. & Beverley-Burton, M.B. (1977) Observations on the seasonal prevalence, pathology and transmission of Dracunculus insignis (Nematoda: Dracunculoidea) in the raccoon (Procyon lotor L.) in Ontario. Journal of Wildlife Diseases 13, 273–280.CrossRefGoogle Scholar
Davies, C., Shelley, J., Harding, P., McLean, I., Gardiner, R. & Peirson, G. (2004) Freshwater fishes in Britain: the species and their distribution. 176 pp. Colchester, Harley Books.CrossRefGoogle Scholar
de Buron, I. & Roumillat, W.A. (2010) Histopathology of two philometrid parasites of the southern flounder, Paralichthys lethostigma. Journal of Wildlife Diseases 46, 277–282.CrossRefGoogle ScholarPubMed
Genc, E., Ayce Genc, M., Genc, E., Cengizler, I. & Faith Can, M. (2005) Seasonal variation and pathology associated with helminths infecting two serranids (Teleostei) of Iskenderun Bay (northeast Mediterranean Sea), Turkey. Turkish Journal of Fisheries and Aquatic Sciences 5, 29–33.Google Scholar
Gollety, C., Connors, V.A., Adams, A.M., Roumillat, W.A. & Buron, I. (2005) Population dynamics of the philometrid nematode Margolisianum bulbosum in the southern flounder Paralichthys lethostigma (Pisces: Paralichthyidae) in South Carolina, USA. Diseases of Aquatic Organisms 65, 69–74.CrossRefGoogle ScholarPubMed
Gulland, F.M.D. (1992) The role of nematode parasites in Soay sheep (Ovis aries L.) mortality during a population crash. Parasitology 105, 493–503.CrossRefGoogle ScholarPubMed
Häenfling, B., Bolton, P., Harley, M., Carvalho, G.R. & Pierson, G. (2005) A molecular approach to detect hybridisation between crucian carp (Carassius carassius) and non-indigenous carp species (Carassius auratus and Cyprinus carpio). Freshwater Biology 50, 403–417.CrossRefGoogle Scholar
Hickley, P. (2009) Recreational fisheries – social, economic and management aspects. pp. 169–189in Ackefors, H. (Ed.) Fisheries, sustainability and development. Stockholm, Royal Swedish Academy of Agriculture and Forestry.Google Scholar
Kaall, S., Sarvala, J. & Fagerholm, H.P. (2001) Prevalence and pathogenicity of the gill artery worm Philometra obturans (Nematoda, Dracunculoidea) of pike (Esox lucius L.) in a lake in SW Finland. Bulletin of the Scandinavian Society for Parasitology 11, 13–14.Google Scholar
Kennedy, C.R. (1994) The ecology of introductions. pp. 189–208in Pike, A.W. & Lewis, J.W. (Eds) Parasitic diseases of fish. Dyfed, Samara Publishing.Google Scholar
Laurila, S., Piironen, J. & Holopainen, I.J. (1987) Notes on egg development and larval and juvenile growth of crucian carp (Carassius carassius (L.)). Annales Zoologici Fennici 24, 315–321.Google Scholar
Lewis, J.W., Jones, D.R. & Adams, J.R. (1974) Functional bursting by the dracunculoid nematode Philonema oncorhynchi. Parasitologia 69, 417–427.CrossRefGoogle ScholarPubMed
Margolis, L. (1970) Nematode diseases of marine fishes. pp. 190–208in Snieszko, S.F. (Ed.) A symposium on diseases of fishes and shellfishes. American Fisheries Society Special Publication 5.Google Scholar
Molnar, K. (1966) On some little-known and new species of the Genera Philometra and Skrjabillanus from fishes in Hungary. Acta Veterinaria Academiae Scietiarum Hungaricae Tomus 16, 143–158.Google ScholarPubMed
Molnar, K., Buchmann, K. & Szekely, C. (2006) Phylum Nematoda. pp. 417–443in Woo, P.T.K. (Ed.) Fish diseases and disorders, Vol. 1. Protozoa and metazoan infections. Cambridge, Massachusetts, CABI Publishing.CrossRefGoogle Scholar
Moravec, F. (1971) Nematodes of fishes in Czechoslovakia. Acta Scientiarum Naturalium Academiae Scientiarum Bohemoslovacae Brno 5, 1–49.Google Scholar
Moravec, F. (1994) Parasitic nematodes of freshwater fishes of Europe. 473 pp. Prague and Dordrecht, Academia and Kluwer Academic Publishers.Google Scholar
Moravec, F. (2004a) Some aspects on the taxonomy and biology of drancunculoid nematodes parasitic in fishes: a review. Folia Parasitologica 51, 1–13.CrossRefGoogle ScholarPubMed
Moravec, F. (2004b) The systematic status of Philometra abdominalis Nybelin, 1928 (Nematoda: Philometridae) ( = a junior synonym of P. ovata Zeder, 1803). Folia Parasitologica 51, 75–76.CrossRefGoogle Scholar
Moravec, F. (2006) Dracunculoid and anguillicoloid nematodes parasitic in vertebrates. 633 pp. Praha, Academia.Google Scholar
Moravec, F. & Cervinka, S. (2005) Female morphology and systematic status of Philometroides cyprini (Nematoda:Philometridae) a parasite of carp. Diseases of Aquatic Organisms 67, 105–109.CrossRefGoogle ScholarPubMed
Moravec, F. & Dykova, I. (1978) On the biology of the nematode Philometra obturans (Prenant, 1886) in the fishpond system of Macha Lake, Czechoslovakia. Folia Parasitologia 29, 227–231.Google Scholar
Moravec, F., Glamuzina, B., Marino, G., Merella, P. & Di Cave, D. (2003) Occurrence of Philometra lateolabracis (Nematoda: Philometridae) in the gonads of marine perciform fishes in the Mediterranean region. Diseases of Aquatic Organisms 53, 267–269.CrossRefGoogle ScholarPubMed
Paperna, I. & Zwerner, D.E. (1976) Parasites and diseases of striped bass, Morone saxatilis (Walbaum), from the lower Chesapeake Bay. Journal of Fish Biology 9, 267–287.CrossRefGoogle Scholar
Saraiva, A., Hermida, M., Costa, M.J., Maia, C., Reis, A.R., Cruz, C. & Valente, A. (2008) First record of Philometra ovata (Nematoda) infection in Gobio lozanoi in Portugal. Journal of Fish Biology 73, 2288–2292.CrossRefGoogle Scholar
Schäperclaus, W., Kulow, H. & Schreckenbach, K. (Eds) (1991) Fish diseases. 5th edn.1398 pp. New Delhi, Oxion Press.Google Scholar
Sekretaryuk, K.V. (1980) Study of transaminase and aldolase activity in Philometroides infection in carp. Doklady Vsesoyuznoy Akademii Sel'skokhozyaystvennykh Nauk V.I. Lenina 11, 37–38(in Russian).Google Scholar
Sekretaryuk, K.V. (1983) Morphological and histochemical changes during Philometroides infection in carp. Veterinariya 9, 45–47(in Russian).Google Scholar
Sinderman, C.J. (1987) Effects of parasites on fish populations: practical considerations. International Journal for Parasitology 17, 371–382.CrossRefGoogle Scholar
Szczerbowski, A., Zakes, Z., Luczynski, M.J. & Szkudlarek, M. (1997) Maturation and growth of a stunted form of crucian carp Carassius carassius L. in natural and controlled conditions. Polish Archive of Hydrobiology 44, 171–180.Google Scholar
Tarkan, A.S., Copp, G.H., Zieba, G., Godard, M.J. & Cucherousset, J. (2009) Growth and reproduction of threatened native crucian carp Carassius carassius in small ponds of Epping Forest, south-east England. Aquatic Conservation: Marine and Freshwater Ecosystems 19, 797–805.CrossRefGoogle Scholar
Uhazy, L.S. (1978) Lesions associated with Philoetroides huronensis (Nematoda: Philometridae) in the white sucker (Catostomus commersoni). Journal of Wildlife Diseases 14, 401–406.CrossRefGoogle ScholarPubMed
Vasilkov, G.V. (1967) Philometrosis of carp. Veterinariya 1, 62–64(in Russian).Google Scholar
Vasilkov, G.V. (1983) Helminthoses of fishes. 208 pp. Moscow, Kolos (in Russian).Google Scholar
Vismanis, K.O. (1966) Study of the agent of philometrosis of carp.Simpozium po parazitam i boleznyam ryb i vodnykh bespozvonochnykh. Tezisy dokladov. pp. 9-10. Moscow-Leningrad, Nauka (in Russian).Google Scholar
Vismanis, K.O (1978) Philometrids (Nematoda, Dracunculoidea) of freshwater fishes of the USSR.Fourth International Congress of Parasitology, August 1978, pp. 186–187 (in Russian).Google Scholar
Vismanis, K.O. & Nikulina, V.N. (1968) Systematic status of Philometra sanguineus (Rudulophi, 1819) (Nematoda, Dracunculidae), a causative agent of philometrosis in crucian carps. Parazitologiya 2, 514–517(in Russian with English summary).Google Scholar
Vismanis, K.O. & Yukhimenko, S.S. (1974) On the morphology of Philometroides dogieli sp. n. (Nematoda: Philometridae) from the fins of Elopichthys bambusa. Parasitologiya 8, 53–56(in Russian with English summary).Google Scholar
Wang, G.T. (2002) Seasonal dynamics and distribution of Philometroides fulvidraconi (Philometroidae) in the bullhead catfish, Pseudobagrus fulvidraco (Richardson). Journal of Fish Diseases 25, 621–625.CrossRefGoogle Scholar
Wheeler, A. (1977) The origin and distribution of the freshwater fishes of the British Isles. Journal of Biogeography 4, 1–24.CrossRefGoogle Scholar
Wheeler, A. (2000) Status of the crucian carp, Carassius carassius (L.) in the UK. Fisheries Management & Ecology 7, 315–322.CrossRefGoogle Scholar
Wierzbicki, K. (1958) Filometroza karasia (Philometrosis carassii). Wiadomosci Parazytologiczne 4, 655–657.Google Scholar
Wierzbicki, K. (1960) Philometrosis of crucian carp. Acta Parasitologica Polonica 8, 181–196.Google Scholar
Williams, H.H. (1967) Helminth diseases of fish. Helminthological Abstracts 36, 261–295.Google Scholar
Yashchuk, V.D. (1971) Life cycle of Philometra sanguineus of carp. Veterinariya 48, 73–75(in Russian).Google Scholar
Yashchuk, V.D. (1974) Dynamics of the infestation of the intermediate hosts of Philometroides sanguinaea. Veterinariya, Moscow 6, 69–71(in Russian).Google Scholar
Yu, Y., Wang, G., Feng, W., Wu, H. & Wang, W. (1993) Philometroidiasis of yellow catfish, Pseudobagrus fulvidraco life cycle of the pathogen and its epidemiology. Transactions of Researchers on Fish Diseases 1, 116–122(in Chinese with English summary).Google Scholar