Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-21T23:48:03.645Z Has data issue: false hasContentIssue false
  • English
  • Français

Anisakis simplex (Rudolphi, 1809, det. Krabbe, 1878) (Nematoda: Ascaridoidea): Morphology and morphometry of larvae from euphausiids and fish, and a review of the life-history and ecology

Published online by Cambridge University Press:  05 June 2009

John W. Smith
John W. Smith
Affiliation:
Marine Laboratory, Aberdeen, Scotland
Get access Rights & Permissions [Opens in a new window]

Abstract

Larval Anisakis 7·7 to 23·6mm long from euphausiids, and larvae 18·0 to 21·9mm long from a teleost fish were morphologically and morphometrically alike and fitted the description by Beverley-Burton, Nyman & Pippy (1977) of A. simplex L3. Three small larvae, 4·2 to 5·9mm long, from euphausiids resembled L3 in anterior but not in posterior morphology; their tails lacked a mucron but, in two of them, cuticular separation at the posterior extremity revealed clearly the mucron characteristic of L3 within. These small larvae are identified as L2 of A. simplex in the process of moulting to L3. Japanese reports of typical L3 from 6·9 to 32·7 mm long in euphausiids, the occurrence in teleosts of typical L3 from only 8·8 to over 30 mm long, and the present observations strongly suggest that the moult from L2 to L3 occurs in euphausiids and begins when the larvae are about 4–6 mm long. Although it appears, therefore, that only one moult occurs in the egg of A. simplex (i.e. ensheathed L2 hatches), two moults there have been reported for various terrestrial and certain aquatic ascaridoids (i.e. ensheathed L3 hatches). The morphology and homology of the lips and associated sense organs of A simplex L3 are discussed relative to that of a ‘typical’ adult ascaridoid.

A main conclusion is that euphausiids in the North-East Atlantic and northern North Sea, and perhaps universally, are major intermediate hosts of A simplex. The status as hosts of squid and teleosts harbouring L3 is discussed. An extensive literature is reviewed in relation to the present observations.

Type
Research Papers
Information
Journal of Helminthology , Volume 57 , Issue 3 , September 1983 , pp. 205 - 224
Copyright
Copyright © Cambridge University Press 1983

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

Allen, J. A. (1959) On the biology of Pandalus borealis Krøyer, with reference to a population off the Northumberland coast. Journal of the Marine Biological Association of the United Kingdom, 38 189–220.CrossRefGoogle Scholar
Araujo, P. (1972a) Observations sur le cycle biologique de l'ascaride Polydelphis quadranqularis (Schneider, 1866) parasite du serpent crotale. Annales de Parasitologie humaine et comparee, 47, 91–120.CrossRefGoogle Scholar
Araujo, P. (1972b) Observačoes pertinentes as primeirasecdises de larvas de Ascaris lumbricoides, A. suum e Toxacara canis. Revista do Instituto de Medicina Tropical de Sào Paulo, 14, 83–90.Google Scholar
Berland, B. (1961) Nematodes from some Norwegian marine fishes. Sarsia, 2, 1–50.Google Scholar
Berry, G. N. & Cannon, L. R. G. (1981) The life history of Sulcascaris sulcata (Nematoda:Ascaridoidea), a parasite of marine molluscs and turtles. International Journal for Parasitology, 11, 43–54.CrossRefGoogle Scholar
Beverley-Burton, M., Nyman, O. L. & Pippy, J. H. C. (1977) The morphology, and some observations on the population genetics of Anisakis simplex larvae (Nematoda: Ascaridata) from fishes of the North Atlantic. Journal of the Fisheries Research Board of Canada, 34, 105–112.CrossRefGoogle Scholar
Bird, A. F. (1971) The Structure of Nematodes. Academic Press, Inc.: New York and London, 318 pp.Google Scholar
Blackburn, M. (1957) The relation between the food of the Australian barracouta, Thyrsites atun (Euphrasen), and recent fluctuations in the fisheries. Australian Journal of Marine and Freshwater Research, 8, 29–54.CrossRefGoogle Scholar
Bruce, R. H. & Aiken, J. (1975) The Undulating Oceanographic Recorder—a new instrument system for sampling plankton and recording physical variables in the euphotic zone from a ship underway. Marine Biology, 32, 85–97.CrossRefGoogle Scholar
Brunsdon, R. V. (1953) A systematic study of the nematodes parasitic in New Zealand marine fish, with an account of the life history and culture of Stomachus marinus (Linn., 1767). M.Sc. Thesis, Victoria University College, Wellington, New Zealand.Google Scholar
Brunsdon, R. V. (1956) Studies on nematode parasites of New Zealand fishes. A systematic and parasitological study of the nematodes occurring in New Zealand marine and fresh-water fishes, including biological studies on the genus Anisakis Dujardin. 1845. Ph.D. Thesis, Victoria University College, Wellington, New Zealand.Google Scholar
Cannon, L. R. G. (1977) Some larval ascaridoids from south-eastern Queensland marine fishes. International Journal for Parasitology, 7, 233–243.CrossRefGoogle ScholarPubMed
Chaubaud, A. G. (1971) Evolution of host parasite adaptation in nematodes of vertebrates. International Journal of Parasitology, 1, 217–221.CrossRefGoogle Scholar
Christiansen, M. E. (1969) Crustacea Decapoda Brachyura. Marine Invertebrates of Scandinavia No. 2, 143 pp. Universitetsforlaget: Oslo, Norway.Google Scholar
Davey, J. T. (1971) A revision of the genus Anisakis Dujardin, 1845 (Nematoda: Ascaridata). Journal of Helminthology, 45, 51–72.CrossRefGoogle Scholar
Deardorff, T. L. & Overstreet, R. M. (1979) Goezia lacerticola sp. n. (Nematoda: Anisakidae) in Alligator mississipprensis from Florida. Journal of Helminthology, 53, 317–320.CrossRefGoogle Scholar
Deardorff, T. L. & Overstreet, R. M. (1980) Taxonomy and biology of North American species of Goezia (Nematoda: Anisakidae) from fishes, including three new species. Proceedings of the Helminthological Society of Washington, 48, 113–126.Google Scholar
Deardorff, T. L. & Overstreet, R. M. (1981 a) Raphidascaris camura sp. n., Hysterothylacium (both previously = Thynnascaris) (Nematoda: Anisakidae) from the northern Gulf of Mexico. Proceedings of the Biological Society of Washington, 93 (Year 1980), 1035–1079.Google Scholar
Deardorff, T. L. & Overstreet, R. M. (1981 b) Larval Hysterothylacium ( = Thynnascaris) (Nematoda: Anisakidae) from fishes and invertebrates in the Gulf of Mexico. Proceedings of the Helminthological Society of Washington, 48, 113–126.Google Scholar
Deardorff, T. L. & Overstreet, R. M. (1981 c) Raphidascaris camura sp. n., Hysterothylacium eurycheilum(Olsen)comb.n., and comments on Heterotyphlum Spaul (Nematoda: Ascaridoidea) in marine fishes. Journal of Parasitology, 67, 426–432.CrossRefGoogle Scholar
De Coninck, L. (1965) Classe des Nématodes. In: Traité de Zoologie: Anatomie, Systematique, Biologic Tome IV, Fasc. II, Nemathelminthes(Nematodes) (Grassé, P.-P., Editor), pp. 3–217. Masson: Paris.Google Scholar
Ekman, S. (1967) Zoogeography of the sea. Sidgwick and Jackson: London.Google Scholar
Fagerholm, H.-P. (1979) Nematode length and preservatives, with a method for determining the length of live specimens. Journal of Parasitology, 65, 334–335.Google Scholar
Gambell, R. (1979) The blue whale. Biologist, 26, 209–215.Google Scholar
Geller, E. R. & Babich, L. A. (1966) Life-cycle of Contracaecum bidentatum (Linstow, 1889). In: Contributions to Helminthology. Published to Commemorate the 75th Birthday of K. I. Skryabin, pp. 133–138. Israel Program for Scientific Translations: Jerusalem. [English translation of 1953 Russian original.]Google Scholar
Gibson, D. I. (1970) Aspects of the development of ‘herring worm’ (Anasakis sp. larva) in experimentally infected rats. Nytt Magasin for Zoologi, 18, 175–187.Google Scholar
Gibson, D.I. (1973) The genus Pseudanisakis Layman and Borovkova, 1926 (Nematoda: Ascaridida). Journal of Natural History, 7, 319–340.Google Scholar
Gibson, D. I. (1983) The systematics of ascaridoid nematodes—a current assessment. In: Concepts in Nematode Systematics(Stone, A. R.Platt, H. M. & Khalil, L. F., Editors). Systematics Association, Special Vol. No. 22, 400 pp. Academic Press Inc.: New York & London.Google Scholar
Grabda, J. (1976) Studies on the life cycle and morphogenesis of Anisakis simplex (Rudolphi, 1809) (Nematoda: Anisakidae) cultured in vitro. Acta Ichthyologica et Piscatoria, 6, 119–141.CrossRefGoogle Scholar
Grainger, J. N. R. (1959) The identity of the larval nematodes found in the body muscles of the cod (Gadus callarias L.). Parasitology, 49, 121–131.CrossRefGoogle ScholarPubMed
Hansen, T. & Berland, B. (1979) Morphology of Anisakis simplex III-stage larva (Nematoda). [Abstract.] Proceedings of the IX Symposium of the Scandinavian Society for Parasitology (Abo, Finland, 11–13 06, 1979), p. 12.Google Scholar
Kagei, N. (1974) [Studies on anisakid nematodes (Anisakinae). IV. Survey of Anisakis larvae in marine Crustacea.] [In Japanese.] Bulletin of the Institute of Public Health, Tokyo, 23, 65–71.Google Scholar
Kagei, N., Asano, K. & Kihata, M. (1978) On the examination against the parasites of Antarctic krill, Euphausia superba. Scientific Report of the Whales Research Institute, Tokyo, No. 30, 311–313.Google Scholar
Kagei, N. & Kureha, K. (1970) [Studies on anisakid Nematoda (Anisakinae) I. Survey of Anisakis sp. on marine mammals collected in the Antarctic Ocean.] [In Japanese.] Bulletin of the Institute of Public Health, Tokyo, 19, 193–196.Google Scholar
Kulachkova, V. G. (1978) The role of herring in the life cycle of Anisakis sp.(Nematoda). [Abstract.] In: 4th International Congress of Parasitology, 19–26 August 1978, Warsaw. Short Communications, Section C. Warsaw, Poland: Organising Committee, p. 195.Google Scholar
Kulachkova, V. G. (1980) [Infection of White Sea herring with larval Anisakis sp. (Nematoda, Ascaridata).] [In Russian.] Parazitologicheskü Sbornik, Leningrad, No. 29, 126–142.Google Scholar
McClelland, G. (1980) Phocanema decipiens: moulting in seals. Experimental Parasitology, 49, 128–136.CrossRefGoogle ScholarPubMed
McClelland, G. & Ronald, K. (1974a) In vitro development of Terranova decipiens (Nematoda) (Krabbe, 1878). Canadian Journal of Zoology, 52, 471–479.Google Scholar
McClelland, G. & Ronald, K. (1974 b) In vitro development of the nematode Contracaecum osculatum Rudolphi 1802 (Nematoda: Anisakinae). Canadian Journal of Zoology, 52, 847–855.CrossRefGoogle ScholarPubMed
Mackintosh, N. A. (1965) The Stocks of Whales. 232 pp. Fishing News (Books) Ltd: London.Google Scholar
Makings, P. (1981) Mesopodopsis slabberi (Mysidacea) at Millport, W. Scotland, with the parasitic nematode Anisakis simplex. Crustaceana, 41, 310–312.Google Scholar
Marshall, N. B. (1979) Developments in Deep-Sea Biology. x + 566 pp. Blandford Press Ltd: Poole, Dorset.Google Scholar
Mauchline, J. (1980) The biology of mysids and euphausiids. Advances in Marine Biology, 18, x + 680 pp.Google Scholar
Mauchline, J. & Fisher, L. R. (1969) The biology of euphausiids. Advances in Marine Biology, 7, ix + 454 pp.CrossRefGoogle Scholar
Maung, M. (1978) The occurrence of the second moult of Ascaris lumbricoides and Ascaris suum. International Journal for Parasitology, 8, 371–378.CrossRefGoogle ScholarPubMed
Myers, B. J. (1975) The nematodes that cause anisakiasis. Journal of Milk and Food Technology, 38, 774–782.Google Scholar
Norris, D. E. & Overstreet, R. M. (1976) The public health implications of larval Thynnascaris nematodes from shellfish. Journal of Milk and Food Technology, 39, 47–54.CrossRefGoogle Scholar
Odening, K. (1976) Conception and terminology of hosts in parasitology. Advances in Parasitology, 14, 1–93.Google Scholar
Oshima, T. (1972) Anisakis and anisakiasis in Japan and adjacent area. In: Progress of Medical Parasitology in Japan (Morishita, K.Komiya, Y.Matsubayashi, H., Editors), Vol. IV, pp. 301–393. Meguro Parasitological Museum: Tokyo.Google Scholar
Oshima, T. (1979) In vitro development of Anisakis larvae collected from fishes caught in Juroshio current and their identification by the adults. [Abstract.] In: XIV Pacific Science Congress, August, 1979. Khabarovsk, USSR. Committee F. Marine Sciences. Section FIII, biological productivity of the Pacific Ocean. Moscow, USSR, p. 291.Google Scholar
Petter, A. J. (1969) Enqûete sur les nématodes des poissons de la région nantaise. Identification des larves d'ascarides parasitant les sardines (en rapport avec les granulomes éosinophiles observés chez l'homme dans la région.. Annales de Parasitologie Humaine et Comparée, 44, 559–580.Google Scholar
Pippy, J. H. C. & Van Banning, P. (1975) Identification of Anisakis larva (1) as Anisakis simplex (Rudolphi, 1809 det. Krabbe, 1878) (Nematoda: Ascaridata). Journal of the Fisheries Research Board of Canada, 32, 29–32.CrossRefGoogle Scholar
Punt, A. (1941) Recherches sur quelques nématodes parasites de poissons de la Mer du Nord. Memoires du Musée Royal d'Histoire Naturelle de Belgigue, No. 98, 110 pp.Google Scholar
Reimer, L. W., Berger, C., Heuer, B., Lainka, H., Rosenthal, I. & Scharnweber, I. (1971) [On the distribution of larvae of helminths in plankton animals of the North Sea.] [In Russian.] Parazitologiya, 5, 542–550.Google Scholar
Reimer, L. W. & Jessen, O. (1972) Parasitenbefall der Nordseeheringe. Angewandte Parasitologie 13, 65–71.Google Scholar
Shimazu, T. & Oshima, T. (1972) Some larval nematodes from euphausiid crustaceans. In: Biological Oceanography of the Northern North Pacific Ocean dedicated to Shigeru Motoda (Takenouti, et al. , Editors) pp. 403–409. Idemitsu Shoten Tokyo, Japan.Google Scholar
Shiraki, T. (1974) Larval nematodes of family Anisakidae (Nematoda) in the Northern Sea of Japan—as a causative agent of eosinophilic phlegmone or granuloma in the human gastro-intestinal tract. Acta Medica et Biologica, Niigata, 22, 57–98.Google Scholar
Shiraki, T., Hasegawa, H. & Kenmotsu, M. (1976) Larval anisakid nematodes from the prawns, Pandalus spp. Japanese Journal of Parasitology, 25, 148–152.Google Scholar
Slijper, E. J. (1962) Whales. 475 pp. Hutchinson and Co. (Publishers) Ltd: London.Google Scholar
Sluiters, J. F. (1974) Anisakis sp. larvae in the stomachs of herring (Clupea harengus L.). Zeitschrift fur Parasitenkunde, 44, 279–288.Google Scholar
Smith, J. W. (1971) Thysanoessa inermis and T. longicaudata (Euphausiidae) as first intermediate hosts of Anisakis sp. (Nematoda: Ascaridata) in the northern North Sea, to the north of Scotland and at Faroe. Nature, London, 234, 478.Google Scholar
Smith, J. W. (1983) Larval Anisakis simplex (Rudolphi, 1809, det. Krabbe, 1878) and larval Hysterothylacium sp. (Nematoda: Ascaridoidea) in euphausiids (Crustacea: Malacostraca) in the North-East Atlantic and northern North Sea. Journal of Helminthology 57, 167–177.Google Scholar
Smith, J. W. & Wootten, R. (1978) Anisakis and anisakiasis. Advances in Parasitology, 16, 93–163.Google Scholar
Soleim, Ø. (1974) Scanning electron microscope observations of Contracaecum aduncum (Nematoda: Ascaridoidea). Norwegian Journal of Zoology, 22, 171–175.Google Scholar
Soleim, Ø. (1976) Morphology of Thynnascaris adunca (Nematoda). [Abstract.] 8th Scandinavian Symposium on Parasitology, Bergen, Norway, 20–22 08 1976.Google Scholar
Sprent, J. F. A. (1969 a) Nematode larva migrans. New Zealand Veterinary Journal, 17, 39–48.CrossRefGoogle ScholarPubMed
Sprent, J. F. A. (1969 b) Helminth “zoonoses”: an analysis. Helminthological Abstracts, 38, 333–351.Google Scholar
Sprent, J. F. A. (1978) Ascaridoid nematodes of amphibians and reptiles: Goezia. Journal of Helminthology, 52, 91–98.Google Scholar
Stephensen, K. (1939) Crustacea Decapoda. Zoology of Iceland 3 (25), 31 pp.Google Scholar
Stephensen, K. (1940) Marine Amphipoda. Zoology of Iceland. 3 (26). 111 pp.Google Scholar
Stephensen, K. (1942) The Amphipoda of North Norway and Spitsbergen with adjacent waters. Tromsø Museums Skrifter, 3, 526 pp.Google Scholar
Suzuki, T. & Ishida, K. (1979) Anisakis simplex and Anisakis physeteris: physicochemical properties of larval and adult hemoglobins. Experimental Parasitology, 48, 225–234.CrossRefGoogle ScholarPubMed
Tambovtsev, B. M. (1959) The biological foundations of the fishery of the White Sea herring. In: The Herring of the North European Basin and Adjacent Seas, pp. 273–284. [Translation from the Russian in US Fish and Wildlife Service, Special Scientific Report—Fisheries No. 327: Washington, D.C.]Google Scholar
Tattersall, W. M. & Tattersall, O. S. (1951) The British Mysidacea. 460 pp. The Ray Society: London.Google Scholar
Thust, R. (1966) Elektronenmikroskopische Untersuchungen uber den Bau des larvalen Integumentes und zur Hautungsmorphologie von Ascaris lumbricoides. Zoologischer Anzeiger 177 411–417.Google Scholar
Thust, R. (1967) Submikroskopische Untersuchungen uber die Morphogenese des Integumentes von Ascaris lumbricoides L. 1758. Zeitschrift fur Wissenschaftliche Zoologie, 178, 1–39.Google Scholar
Uspenskaya, A. V. (1963) [Parasite fauna of benthic crustaceans from the Barents Sea.] [In Russian.] 127 pp. Izdatel'stvo Akademiya Nauk SSSR: Moscow and Leningrad.Google Scholar
Val'ter, E. D. & Popova, T. I. (1974) [The role of the polychaete Lepidonotus squamatus L. in the biology of anisakids.] [In Russian.] Trudy Belomorskogo Biologicheskoi Stantsii Moskovskogo Gosudarstvennogo Universiteta, 4, 177–182.Google Scholar
Van Banning, P. (1967) Nematodes in plankton samples from the North Sea. International Council for the Exploration of the Sea, Pelagic Fish (Northern) Committee. Ref. Plankton Committee, CM 1967/H: 20, 5 pp. (mimeo.).Google Scholar
Van Banning, P. & Becker, H. B. (1978) Long-term survey data (1965–1972) on the occurrence of Anisakis larvae (Nematoda: Ascaridida) in herring, Clupea harengus L., from the North Sea. Journal of Fish Biology, 12, 25–33.CrossRefGoogle Scholar
Walter [val'ter], E. D. (1978) Scanning electron microscopy of anisakid larvae. [Abstract] In: 4th International Congress of Parasitology, 19–26 August, 1978. Warsaw. Short Communications, Section B. Warsaw, Poland: Organising Committee, p. 50.Google Scholar
Warren, E. G. (1971) A new species of Toxascaris from hyenas. Parasitology, 62, 171–178.Google Scholar
Webb, B. F. (1976) Aspects of the biology of jack mackerel, Trachurus declivis (Jenyns) from south-east Australian waters. Tasmanian Fisheries Research, 10, 1–14.Google Scholar
Williams, H. H. & Richards, D. H. H. (1968) Observations on Pseudanisakis rotundata (Rudolphi, 1819) Mozgovoi, 1950, a common but little known nematode parasite of Raia radiata Donovan in the Northern North Sea. Journal of Helminthology, 42, 199–219.CrossRefGoogle Scholar
Wootten, R. & Smith, J. W. (1975) Observational and experimental studies on the acquisition of Anisakis sp. larvae (Nematoda: Ascaridida) by troug in fresh water. International Journal for Parasitology, 5, 373–378.CrossRefGoogle Scholar
Wright, K. A. (1980) Nematode sense organs. In: Nematodes as Biological Models, Volume 2. Aging and other Model Systems. (Zuckerman, B. M., Editor) pp. 237–295. Academic Press, Inc: New York and London.Google Scholar