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Life cycles of species of Proteocephalus, parasites of fishes in the Palearctic Region: a review

Published online by Cambridge University Press:  11 April 2024

T. Scholz*
Affiliation:
Institute of Parasitology,Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 Ceské Budějovice, Czech Republic
*
*Fax: +420 38 47743, Email [email protected]
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Abstract

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The life cycles of species of Proteocephalus Weinland, 1858 (Cestoda: Proteocephalidea) parasitizing fishes in the Palearctic Region are reviewed on the basis of literary data and personal experimental observations, with special attention being paid to the development within the intermediate and definitive hosts. Planktonic crustaceans, diaptomid or cyclopid copepods (Copepoda), serve as the only intermediate hosts of all Proteocephalus species considered. A metacestode, or procercoid, develops in the body cavity of these planktonic crustaceans and the definitive host, a fish, becomes infected directly after consuming them. No previous reports of the parenteral location of metacestodes within the second intermediate host as it is in the Nearctic species P. ambloplitis have been recorded. Thus, the life cycles of Proteocephalus tapeworms resemble in their general patterns those of some pseudophyllidean cestodes such as Eubothrium or Bothriocephalus, differing from the latter in the presence of a floating eggs instead of possessing an operculate egg from which a ciliated, freely swimming larva, a coracidium, is liberated. The scolex of Proteocephalus is already formed at the stage of the procercoid within the copepod intermediate host; in this feature, proteocephalideans resemble caryophyllidean rather than pseudophyllidean cestodes. The morphology of procercoids of individual species is described with respect to the possibility of their differentiation and data on the spectrum of intermediate hosts are summarized. Procercoids of most taxa have a cercomer, which does not contain embryonic hooks in contrast to most pseudophyllidean cestodes. The role of invertebrates (alder-fly larvae — Megaloptera) and small prey fishes feeding upon plankton in the transmission of Proteocephalus tapeworms still remains unclear but these hosts are likely to occur in the life cycle. Data on the establishment of procercoids in definitive hosts, morphogenesis of tapeworms within fish hosts, and the length of the prepatent period are still scarce and new observations are needed. Whereas extensive information exists on the development of P. longicollis (syns. P. exiguus and P. neglectus), almost no data are available on the ontogeny of other taxa, in particular those occurring in brackish waters (P. gobiorum, P. tetrastomus). The morphology of P. cernuae and P. osculatus procercoids from experimentally infected intermediate hosts is described for the first time.

Type
Review Article
Copyright
Copyright © Cambridge University Press 1999

References

Albetova, L.M.(1975) On the proteocephalosis of white fish from Kuchak Lake of the Lower Tabdinsk group of the Tyumen Region. Izvestiya Gossudarstvenogo Nauchno-issledovatelskogo Instituta Ozernogo i Rechnogo Rybnogo Khozyaistva 93, 105107. (In Russian.)Google Scholar
Albetova, L.M.(1976) On the reproduction of life cycle in Proteocephalus exiguus La Rue, 1911 (Cestoda, Proteocephalidae) under experimental conditions. Nauchnye Trudy Tyumenskogo Universiteta 31, 117124. (In Russian.)Google Scholar
Andersen, K.(1979) Variation in scolex morphology within and between some species of the genus Proteocephalus Weinland (Cestoda, Proteocephala) with to strobilar morphology. Zoologica Scripta 8, 241248.CrossRefGoogle Scholar
Andersen, K.I. & Valtonen, E.T.(1990) On the infracommunity structure of adult cestodes in freshwater fishes. Parasitology 101, 257264.CrossRefGoogle ScholarPubMed
Anikieva, L.V.(1982) The development of proteocephalus exiguus in intermediate hosts. pp. 114128 in Shulman, S.S. (Ed.) Ekologiya paraziticheskikh organizmov v biogeotsenozakh severa. Petrozavodsk. (In Russian.)Google Scholar
Anikieva, L.V.(1992a) Morphological variability of the population of Proteocephalus percae (Cestoda: Proteocephalidae) from lake Rindozero. Parazitologiya 26, 389395. (In Russian.)Google Scholar
Anikieva, L.V.(1992b) Population morphology of Proteocephalus torulosus (Cestoda, Proteocephalidae) from cyprinids of the Karelian lakes. Ecological Parasitology 1, 135149.Google Scholar
Anikieva, L.V.(1993) Morphological diversity of the populations of Proteocephalus percae (Proteocephalidae) in water bodies of Karelia. Parazitologiya 27, 260268. (In Russian.)Google ScholarPubMed
Anikieva, L.V.(1995) Variability of a perch's parasite Proteocephalus percae in the areal of the host. Parazitologiya 29, 279288. (In Russian.)Google Scholar
Anikieva, L.V. & Malakhova, R.P.(1975) Peculiarities of the development of the cestode Proteocephalus exiguus in relation to environmental conditions. Osnovy bioproduktsii vnutrennykh vod Pribaltiki, Vilnius, pp. 401402. (In Russian.)Google Scholar
Anikieva, L.V.,Malakhova, R.P.& Ieshko, E.P.(1983) Ecological analysis of parasites of coregonid fish. 168 pp. Leningrad, Publ. House Nauka. (In Russian.)Google Scholar
Balling, T.E. & Pfeiffer, W.(1997) Frequency distributions of fish parasites in the perch Perca fluviatilis L. from Lake Constance. Parasitology Research 83, 370373.CrossRefGoogle ScholarPubMed
Befus, A.D. & Freeman, R.S.(1973a) Corallobothrium parafimbriatum sp. n. and Corallotaenia minutia (Fritts, 1959) comb. n. (Cestoda: Proteocephaloidea) from Algonquin Park, Ontario. Canadian Journal of Zoology 51, 243248.CrossRefGoogle Scholar
Befus, A.D. & Freeman, R.S.(1973b) Life cycles of two corallobothriin cestodes (Proteocephaloidea) from Algonquin Park, Ontario.Canadian Journal of Zoology 51, 249257.CrossRefGoogle ScholarPubMed
de Chambrier, A. & Rego, A.A.(1995) Mariauxiella pimelodi n.g., n.sp. (Cestoda: Monticelliidae): a parasite of pimelodid siluroid fishes from South America. Systematic Parasitology 30, 5765.CrossRefGoogle Scholar
de Chambrier, A. &, Vaucher, C.(1994) Etude morpho-anatomique et génétique de deux nouveaux Proteocephalus Weinland, 1858 (Cestoda: Proteocephalidae) parasites de Platydoras costatus(L.), poisson siluriforme du Paraguay. Systematic Parasitology 27, 173185.CrossRefGoogle Scholar
Chubb, J.C.(1982) Seasonal occurrence of helminths in freshwater fishes. Part IV. Adult Cestoda, Nematoda and Acanthocephala. Advances in Parasitology 20, 1292.CrossRefGoogle ScholarPubMed
Chubb, J.C., Pool, D.W. & Veltkamp, C.J.(1987) A key to the species of cestodes (tapeworms) parasitic in British and Irish freshwater fishes. Journal of Fish Biology 31, 517543.CrossRefGoogle Scholar
Cooper, A.R.(1915) Contributions to the life history of Proteocephalus ambloplitis Leidy, a parasite of the black bass. Contributions in Canadian Biology 2, 177194.Google Scholar
Doby, J.M. & Jarecka, L.(1964) Redescription d'un Proteocephalus (Cestode) parasite du poisson Coregonus fera en provenance du lac Léman. Problèmes posés par la diagnose spécifique des Cestodes du genre Proteocephalus . Bulletin de la Societé de Zoologie Francaise 89, 675687.Google Scholar
Doby, J.M. & Jarecka, L.(1966) Complément a la connaissance de la morphologie et de la biologie de Proteocephalus macrocephalus (Creplin, 1825), cestode parasite de l'anguille. Annales de Parasitologie Humaine et Comparée 41, 429442.CrossRefGoogle Scholar
Dubinina, M.N.(1952) Some remarks on the classification of tapeworms of the family Proteocephalidae La Rue and their distribution in the USSR Parazitologicheskii sbornik, Zoological Institute of Academy of Sciences of the USSR, 14, 281302. (In Russian.)Google Scholar
Dubinina, M.N.(1980) Tapeworms (Cestoda, Ligulidae) of the fauna of the USSR. 320 pp. Translation from Russian, New Delhi, Amerind Publ. Co.Google Scholar
Dubinina, M.N.(1987) Class Cestoda Rudolphi, 1808. pp. 576 in Bauer, O.N (Ed.) Key to the parasites of freshwater fishes of the USSR. Vol. 3. Leningrad, Publ. House Nauka. (In Russian.)Google Scholar
Dupont, F. & Gabrion, C.(1986) Approche expérimentale du role de l'hôte paraténique dans la circulation du parasite Bothriocephalus claviceps Goeze, 1782 (Cestoda, Pseudophyllidea). Annales de Parasitologie Humaine et Comparée 61, 423429.CrossRefGoogle Scholar
Essex, H.E.(1927) The structure and development of Corallobothrium. Illinois Biological Monographs 11, 257328.Google Scholar
Eure, H.(1976) Seasonal abundance of Proteocephalus ambloplitis (Cestoidea Proteocephalidea) from largemouth bass living in heated reservoir. Parasitology 73, 205212.CrossRefGoogle ScholarPubMed
Euzet, L., Swiderski, Z. & Mokhtar-Maamouri, F.(1981) Ultrastructure comparée du spermatozoïde des cestodes. Relations avec la phylogenèse. Annales de Parasitologie Humaine et Comparée 56, 247259.CrossRefGoogle Scholar
Fischer, H.(1968) The life cycle of Proteocephalus fluviatilis Bangham (Cestoda) from smallmouth bass, Micropterus dolomieui Lacépède. Canadian Journal of Zoology 46, 569579.CrossRefGoogle Scholar
Fischer, H. & Freeman, R.S.(1969) Penetration of parenteral plerocercoids of Proteocephalus ambloplitis (Leidy) into the gut of smallmouth bass. Journal of Parasitology 55, 766774.CrossRefGoogle Scholar
Fischer, H. & Freeman, R.S.(1973) The role of plerocercoids in the biology of Proteocephalus ambloplitis (Cestoda) maturing in smallmouth bass. Canadian Journal of Zoology 51, 133141.CrossRefGoogle ScholarPubMed
Freeman, R.S.(1964) On the biology of Proteocephalus parallacticus MacLulich (Cestoda) in Algonquin Park, Canada.Canadian Journal of Zoology 42, 387408.CrossRefGoogle Scholar
Freeman, R.S.(1973) Ontogeny of cestodes and its bearing on their phylogeny and systematics. Advances in Parasitology 11, 481557.CrossRefGoogle ScholarPubMed
Freze, V.I.(1965a) Proteocephalids — tapeworm helminths of fish, amphibians and reptiles. Essentials of Cestodology, vol. V. 540 pp. Moscow, Publ. House Nauka. (In Russian.)Google Scholar
Freze, V.I.(1965b) Ontogenetic stages and developmental cycles of proteocephalideans (Cestoda, Proteocephalata). Trudy GELAN 15, 185195. (In Russian.)Google Scholar
Gresson, R.A.R.(1962) Spermatogenesis of Cestoda. Nature, 194, 397398.CrossRefGoogle Scholar
Gruber, A.(1878) Ein neuer Cestoden-Wirt. Zoologischer Anzeiger 1, 7475.Google Scholar
Gulyaev, V.D.(1997) Classification of metacestodes as a system of life-forms characteristic to cestode parasitic larvae.Byulletin Moskovskogo Obshchestva Ispitatelei Prirody, Otdelenie Biologii 102, (2), 2633. (In Russian.)Google Scholar
Hanzelová, V.(1992) Proteocephalus neglectus as a possible indicator of changes in the ecological balance of aquatic environments.Journal of Helminthology 66, 1724.CrossRefGoogle Scholar
Hanzelová, V. & Scholz, T.(1993) Systematic status of Proteocephalus tumidocollis (Cestoda: Proteocephalidae), a parasite of salmonid fishes in North America. Helminthologia 30, 157161.Google Scholar
Hanzelová, V., Špakulová, M.(1992) Biometric variability of Proteocephalus neglectus (Cestoda: Proteocephalidae) in two different age groups in the rainbow trout from the Dobšiná dam (East Slovakia). Folia Parasitologica 39, 307316.Google Scholar
Hanzelová, V., Zitnan, R. & Sysoev, A.V.(1988) Invasion cycle of Proteocephalus neglectus La Rue, 1911 (Cestoda). European Multicolloquium of Parasitology, Sept. 4–9, 1988, Budapest, Hungary. Programme and Abstracts, p. 192.Google Scholar
Hanzelová, V., Sysoev, A.V.&, Zitnan, R.(1989) Ecology of Proteocephalus neglectus La Rue, 1911 (Cestoda) in the stage of procercoid in Dobšiná dam (East Slovakia) .Helminthologia 26, 105116.Google Scholar
Hanzelová, V., Zitnan, R.&, Sysoev, A.V.(1990) The seasonal dynamics of invasion cycle of Proteocephalus neglectus (Cestoda) Helminthologia 27, 135144.Google Scholar
Hanzelová, V., Scholz, T. & Fagerholm, H.P.(1995a) Synonymy of Proteocephalus neglectus La Rue, 1911 with P. exiguus La Rue, 1911, two fish cestodes from the Holarctic Region. Systematic Parasitology 30, 173185.CrossRefGoogle Scholar
Hanzelová, V., Šnábel, V., Špakulová, M., Králová, I. & Fagerholm, H.P.(1995b) A comparative study of the fish parasites Proteocephalus exiguus and P. percae (Cestoda: Proteocephalidae): morphology, isoenzymes, and karyotype. Canadian Journal of Zoology 73, 11911198.CrossRefGoogle Scholar
Hanzelová, V., Šnábel, V., Špakulová, M. & Králová, I.(1996) On the host specificity of species of Proteocephalus (Cestoda: Proteocephalidae) Parasite 4, 321327.Google Scholar
Hilliard, D.K.(1960) The taxonomic significance of eggs and coracidia of some diphyllobothriid cestodes. Journal of Parasitology 46, 703716.CrossRefGoogle Scholar
Hoberg, E.P., Mariaux, J., Justine, J.L., Brooks, D.R. & Weekes, P.J.(1997) Phylogeny of the orders of the Eucestoda (Cercomeromorphae) based on comparative morphology: historical perspectives and a new working hypothesis.Journal of Parasitology 83, 11281147.CrossRefGoogle Scholar
Hopkins, C.A.(1959) Seasonal variations in the incidence and development of the cestode Proteocephalus filicollis (Rud., 1810) in Gasterosteus aculeatus(L.). Parasitology 49, 529542.CrossRefGoogle ScholarPubMed
Hunter, G.W.(1928) Contribution to the life-history of Proteocephalus ambloplitis (Leidy). Journal of Parasitology, 14, 229242.CrossRefGoogle Scholar
Hunter, G.W.(1929) Life-history studies on Proteocephalus pinguis La Rue. Parasitology 19, 487490.CrossRefGoogle Scholar
Hunter, G.W. & Hunninen, A.V.(1934) Studies on the plerocercoid larva of the bass tapeworm, Proteocephalus ambloplitis (Leidy), in the small-mouthed bass. Supplement of the 23rd Annual Report. New York State Conservation Department, 1933, No. 8, 255–261.Google Scholar
Ieshko, Y.P.(1980) Polymorphism of embryonic hooks of oncospheres in cestodes of the genera Proteocephalus and Eubothrium. Parazitologiya 14, 5660. (In Russian.)Google Scholar
Janicki, C. & Rosen, F.(1917) Le cycle évolutif du Dibothriocephalus latus L. Bulletin de la Société Neuchatelaise de Sciences Naturelles 42, 1953.Google Scholar
Jarecka, L.(1956) Larwy tasiemcow w jeziorze GoldapiwoWiadomoszci. Parazytologiczne 11, 203204.Google Scholar
Jarecka, L.(1960) Life cycles of tapeworms from lakes Goldapiwo and Mamry PolnoczneActa. Parasitologica Polonica 8, 4766.Google Scholar
Jarecka, L.(1975) Ontogeny and evolution of cestodesActa. Parasitologica Polonica 23, 93114.Google Scholar
Jarecka, L. & Doby, J.M.(1965) Contribution a l'étude du cycle évolutif d'un cestode du genre Proteocephalus parasite de Coregonus fera en provenance du Lac Léman. Annales de Parasitologie Humaine et Comparée 40, 433443.CrossRefGoogle Scholar
Joyeux, C. & Baer, J.G.(1961) Classe de Cestodes. pp. 347560 in Grassé, P.P. (Ed.) Traité de Zoologie. vol. 4, Paris, Masson.Google Scholar
Justine, J.-L.(1998) Spermatozooa as phylogenetic characters for the Eucestoda. Journal of Parasitology 84, 385408.CrossRefGoogle Scholar
Kataoka, N. & Momma, K.(1935) A preliminary note on the life-history of Proteocephalus neglectus, with special to its intermediate host.Bulletin of the Japanese Society of Scientific Fisheries 3, 125126.CrossRefGoogle Scholar
Kearn, G.C.(1998) Parasitism and the platyhelminths. 544 pp. London, Chapman & Hall.Google Scholar
Kennedy, C.R. & Hine, P.M.(1969) Population biology of the cestode Proteocephalus torulosus (Batsch) in dace Leuciscus leuciscus (L.) of the River Avon.Journal of Fish Biology 1, 209219.CrossRefGoogle Scholar
Kennedy, C.R., Nie, P. & Rostron, J.(1992) An insect, Sialis lutaria, as a host for larval Proteocephalus sp.Journal of Helminthology 66, 716.CrossRefGoogle Scholar
Kuczkowski, S.(1925) Die Entwicklung im Genus Ichthyotaenia Lönnb. Ein Beitrag zur Cercomertheorie auf Grund experimenteller Untersuchungen. Bulletin de l'Academie Polonaise de Sciences, Série B, 423446.Google Scholar
Kuperman, B.I.(1973) Tapeworms of the genus Triaenophorus, parasites of fishes. 208 pp. Leningrad, Nauka. (In Russian.)Google Scholar
La, Rue, G.R.(1914) A revision of the cestode family Proteocephalidae. Illinois Biological Monographs 1, No. 1–2, pp. 3351.Google Scholar
Llewellyn, J.(1965) The evolution of parasitic platyhelminths. pp. 4778 in Taylor, A.E.R. (Ed.) Evolution of parasites. Third Symposium of the British Society for Parasitology. Oxford, Blackwells.Google Scholar
Mackiewicz, J.S.(1972) Parasitological review. Caryophyllidea (Cestoidea). Experimental Parasitology 31, 417512.CrossRefGoogle Scholar
Mackiewicz, J.S.(1988) Cestode transmission patterns. Journal of Parasitology 74, 6071.CrossRefGoogle ScholarPubMed
Malakhova, R.P. & Anikieva, L.V.(1976) On the biology of Proteocephalus exiguus in fishes from subfamily Coregonidae. Parasitological studies in Karelian ASSR and Murmansk Region, Petrozavodsk, pp. 168175. (In Russian.)Google Scholar
Marcogliese, D.J.(1995) The role of zooplankton in the transmission of helminth parasites to fish. Reviews in Fish Biology and Fisheries 5, 336371.CrossRefGoogle Scholar
Mariaux, J.(1996) Cestode systematics: any progress? International Journal for Parasitology 26, 231243.CrossRefGoogle ScholarPubMed
Mariaux, J.(1998) A molecular phylogeny of the Eucestoda.Journal of Parasitology 84, 114124.CrossRefGoogle ScholarPubMed
Markevich, G.I. & Kuperman, B.I.(1982) Natural infection of copepods with procercoids of tapeworms in a water reservoir in relation to different ecological conditions. Helminths in freshwater biocenoses, Nauka, Moscow, pp. 113122. (In Russian.)Google Scholar
Meggitt, F.J.(1914) The structure and life history of a tapeworm (Ichthyotaenia filicollis Rud.) in the stickleback.Proceedings of the Zoological Society, London, 1914, 113138.Google Scholar
Molnár, K.(1968) Untersuchungen über die jahreszeitlichen Schwankungen in der Parasitenfauna des Kaulbarsches und des Zanders im Balaton mit besonderer Berücksichtigung der Gattung Proteocephalus. Angewandte Parasitologie 7, 6577.Google Scholar
Molnár, K. & Murai, E.(1978) Proteocephalidea scolexek elöfordulása pontynak mint paratenikus gazdának a hasüregében. Parasitologia Hungarica, 11, 143144.Google Scholar
Morandi, H. & Ponton, D.(1989) Cycle évolutif d'un cestode Proteocephalidae parasite du corégone du Lac Léman (Coregonus lavaretus L.) Annales de Parasitologie Humaine et Comparée 64, 257267.CrossRefGoogle Scholar
Moravec, F.(1979) Occurrence of the endoparasitic helminths in pike (Esox lucius L.) from the Mácha Lake fishpond system. Vestník Ceskoslovenské Spolecnosti Zoologické 43, 174193.Google Scholar
Moravec, F., Konecny, R., Molnár, K., Rydlo, M., Scholz, T., Baska, F. & Schiemer, F.(1997) Endohelminth fauna of barbel, Barbus barbus (L.), under ecological conditions of the Danube basin in Central Europe. Studies of Academy of Sciences of the Czech Republic, No. 3, 96 pp. Academia Praha.Google Scholar
Moravec, F. & Škoríková, B.(1998) Amphibians and larvae of aquatic insects as new paratenic hosts of Anguillicola crassus (Nematoda: Dracunculoidea), a swimbladder parasite of eels. Diseases of Aquatic Organisms (in press).CrossRefGoogle ScholarPubMed
Mrázek, A.(1891) Contributions to the studies on some tapeworms of birds. Vestník Královské Ceské Spolecnosti Nauk 1891, 97131. (In Czech.)Google Scholar
Mrázek, A.(1917) On a larva of the tapeworm Ichthyotaenia torulosa . Sborník Zoologický 1, 1117. (In Czech.)Google Scholar
Nie, P. & Kennedy, C.R.(1991) Population biology of Proteocephalus macrocephalus (Creplin) in the European eel, Anguilla anguilla (Linnaeus), in two small rivers. Journal of Fish Biology 38, 921927.CrossRefGoogle Scholar
Odening, K.(1976) Conception and terminology of hosts in parasitology. Advances in Parasitology 14, 193.CrossRefGoogle ScholarPubMed
Priemer, J.(1980)Zum Lebenszyklus von Proteocephalus neglectus (Cestoda) aus Regenbogenforellen Salmo gairdneri Angewandte Parasitologie 21, 125133.Google Scholar
Priemer, J.(1982) Bestimmung von Fischbandwürmern der Gattung Proteocephalus (Cestoda: Proteocephalidae) in Mitteleuropa. Zoologischer Anzeiger 208, 244264.Google Scholar
Priemer, J.(1987) On the life-cycle of Proteocephalus exiguus (Cestoda) from Salmo gairdneri (Pisces).Helminthologia 24, 7585.Google Scholar
Priemer, J. & Goltz, A.(1986) Proteocephalus exiguus (Cestoda) als Parasit von Salmo gairdneri (Pisces). Angewandte Parasitologie 27, 157168.Google ScholarPubMed
Pronina, S.V. & Pronin, N.M.(1988) Interrelationships in systems helminths–fishes (at tissue, organ and organismal levels). Nauka, Moscow, 177 pp. (In Russian.)Google Scholar
Prouza, A.(1978) The life cycle of the tapeworm Proteocephalus neglectus La Rue, 1911. Sborník vedeckých prací ÚSVÚ, Praha, 8, 5663. (In Czech, with English, Russian and Spanish summaries.)Google Scholar
Rego, A.A.(1994) Order Proteocephalidea Mola, 1928. pp. 257293 in Khalil, L.F., Jones, A. & Bray, R.A. (eds.) Keys to the cestode parasites of vertebrates. Wallingford, Oxon, CAB International.Google Scholar
Rego, A.A., de Chambrier, A., Hanzelová, V., Hoberg, E., Scholz, T., Weekes, P. & Zehnder, M.(1998) Preliminary phylogenetic analysis of subfamilies of the Proteocephalidea (Cestoda). Systematic Parasitology 40, 119.CrossRefGoogle Scholar
Rintamäki, P. & Valtonen, E.T.(1988) Seasonal and size-bound infection of Proteocephalus exiguus in four coregonid species in northern Finland. Folia Parasitologica 35, 317328.Google Scholar
Rusinek, O.T.(1986) Variability of oncosphere hooks of the genus Proteocephalus (Cestodes, Proteocephalidae) parasites of Baikal Lake fishes. Proceedings of the Zoological Institute, Leningrad, 155, 128133. (In Russian.)Google Scholar
Rusinek, O.T.(1987a) Cestodes of the genus Proteocephalus, parasites of fishes in the Lake Baikal. Parazitologiya 21, 127133. (In Russian.)Google Scholar
Rusinek, O.T.(1987b) Zum Lebenszyklus von Proteocephalus exiguus (Cestoda) im BaikalseeAngewandte. Parasitologie 28, 3336.Google Scholar
Rusinek, O.T.(1989) The life cycle of Proteocephalus thymalli (Cestoda, Proteocephalidae), a parasite of Siberian glame from Lake Baikal. Parazitologiya 26, 518523. (In Russian.)Google Scholar
Rusinek, O.T. & Pronin, N.M.(1991) Proteocephalus thymalli (Annenkowa-Chlopina, 1923) and P. exiguus La Rue, 1911. pp. 92110 in Dynamics of animal infections by worms. Ulan-Ude. (In Russian.)Google Scholar
Rusinek, O.T., Bakina, M.P. & Nikolskii, A.V.(1996) Natural infection of the calanoid crustacean Epischura baicalensis by procercoids of Proteocephalus sp. in Listvenichnyi Bay, Lake BaikalJournal of Helminthology 70, 237247.Google Scholar
Rybicka, K.(1966) Embryogenesis in cestodesAdvances in. Parasitology 4, 107186.Google Scholar
Schmidt, G.D.(1986) Handbook of tapeworm identification. 675 pp. Boca Raton, Florida, CRC Press.Google Scholar
Scholz, T.(1986) Observations on the ecology of five species of intestinal helminths in perch (Perca fluviatilis) from the Mácha Lake fishpond system, Czechoslovakia. Vestník Ceskoslovenské Spolecnosti Zoologické 50, 300320.Google Scholar
Scholz, T.(1989a) Amphilinida and Cestoda, parasites of fish in CzechoslovakiaActa Scientiarum Naturalium, Brno, 23, No. 4, 56 pp.Google Scholar
Scholz, T.(1989b) On the ecology of the cestode Proteocephalus torulosus (Batsch, 1786) in chub (Leuciscus cephalus L.) from the river Rokytná, Czechoslovakia. Helminthologia 26, 275285.Google Scholar
Scholz, T.(1991a) Studies on the development of the cestode Proteocephalus neglectus La Rue, 1911 (Cestoda: Proteocephalidea) under experimental conditionsFolia. Parasitologica 38, 3955.Google Scholar
Scholz, T.(1991b) Early development of Khawia sinensis Hsü, 1935 (Cestoda: Caryophyllidea)Folia. Parasitologica 38, 133142.Google Scholar
Scholz, T.(1993a) Development of Proteocephalus torulosus (Batsch, 1786) (Cestoda: Proteocephalidae) in the intermediate host under experimental conditions. Journal of Helminthology 67, 316324.CrossRefGoogle ScholarPubMed
Scholz, T.(1993b) On the development of Khawia baltica Szidat, 1942 (Cestoda, Lytocestidae), a parasite of tench (Tinca tinca (L.)).Folia Parasitologica 40, 99104.Google Scholar
Scholz, T.(1997) Life-cycle of Bothriocephalus claviceps, a specific parasite of eels. Journal of Helminthology 71, 241252.CrossRefGoogle ScholarPubMed
Scholz, T. & Hanzelová, V.(1998) Tapeworms of the genus Proteocephalus Weinland, 1858 (Cestoda: Proteocephalidae), parasites of fishes in Europe. Studies of the Academy of Sciences, No. 2, 120 pp. Academia, Praha.Google Scholar
Scholz, T. & Moravec, F.(1993) Finding of Proteocephalus sp. larva (Cestoda: Proteocephalidae) in Sialis lutaria (Insecta: Megaloptera). ActaSocietatis Zoologicae Bohemoslovacae 57, 159160.Google Scholar
Scholz, T. & Moravec, F.(1994) Life history of Proteocephalus torulosus (Cestoda: Proteocephalidae) in barbel (Barbus barbus) from the Jihlava River, Czech Republic. Folia Parasitologica 41, 253257.Google Scholar
Scholz, T., Špakulová, M., Šnábel, V., Králová, I. & Hanzelová, V.(1997) A multidisciplinary approach to the systematics of Proteocephalus macrocephalus (Cestoda: Proteocephalidae). Systematic Parasitology 37, 112.CrossRefGoogle Scholar
Scholz, T., Drábek, R. & Hanzelová, V.(1998a) Scolex morphology of Proteocephalus tapeworms (Cestoda: Proteocephalidae), parasites of freshwater fish in the Palaearctic Region. Folia Parasitologica 45, 2739.Google ScholarPubMed
Scholz, T., Hanzelová, V., Králová, I. & Griffiths, D.(1998b) Synonymization of Proteocephalus pollanicola Gresson, 1952 (Cestoda: Proteocephalidae), a parasite of pollan, Coregonus autumnalis pollanicola, with P. exiguus La Rue, 1911. Systematic Parasitology 40, 3541.CrossRefGoogle Scholar
Shulman, S.S.(1954) On the specificity of fish parasites. Zoologicheskii Zhurnal 33, 1425.Google Scholar
Smyth, J.D.(1994) Introduction to animal parasitology. Third edition. 549 pp. Cambridge, Cambridge University Press.Google Scholar
Smyth, J.D. & McManus, D.P.(1989) The physiology and biochemistry of cestodes. 398 pp. Cambridge, Cambridge University Press.CrossRefGoogle Scholar
Šnábel, V., Hanzelová, V. & Fagerholm, H.P.(1994) Morphological and genetic comparison of two Proteocephalus species (Cestoda: Proteocephalidae) Parasitology Research 80, 141146.CrossRefGoogle ScholarPubMed
Šnábel, V., Hanzelová, V., Mattiucci, S., D'Amelio, S. & Paggi, L.(1996) Genetic polymorphism in Proteocephalus exiguus shown by enzyme electrophoresis.Journal of Helminthology 70, 345349.CrossRefGoogle Scholar
Stunkard, H.W.(1967) Platyhelminth parasites of invertebrates. Journal of Parasitology 53, 673682.CrossRefGoogle ScholarPubMed
Swiderski, Z.(1985) Spermiogenesis in the proteocephalid cestode Proteocephalus longicollis. pp. 181182 in Timme, A.H. (Ed.) Proceedings of the Electron Microscopical Society of South Africa, 24 Annual Conference, 4–6 December 1985,University of Natal, Pietermaritzburg,Pietermaritzburg, Republic of South Africa. Google Scholar
Swiderski, Z.(1996) Fertilization in proteocephalid cestode Proteocephalus longicollis (Zeder, 1800). pp. 495–496 in Cottell, D. & Steer, M. (Eds) Proceedings of the 11th European Congress on Electron Microscopy, 26–30 August 1996, Dublin, Ireland.Google Scholar
Swiderski, Z. & Eklu-Natey, R.D.(1978) Fine structure of the spermatozoon of Proteocephalus longicollis (Cestoda, Proteocephalidea). pp. 572573 in Brederoo, P. & Priester, W. (Eds) Proceedings of the 9th International Congress of Electron Microscopy, 1–9 August 1978, Toronto, Canada.Google Scholar
Swiderski, Z. & Eklu-Natey, R.D., Subilia, L. & Huggel, H.(1978) Comparative fine structure of vitelline cells in the cestode Proteocephalus longicollis (Proteocephalidea). pp. 669–670 in Brederoo, P. & Priester, W. (Eds.) Proceedings of the 9th International Congress of Electron Microscopy, 1–9 August 1978, Toronto, Canada.Google Scholar
Sysoev, A.V.(1983) The composition of intermediate hosts of Proteocephalus torulosus (Batsch) (Cestoda: Proteocephalidae) and the dynamics of invasion of Copepoda with this parasite under conditions of Karelia. Helminthologia 20, 97102.Google Scholar
Sysoev, A.V.(1985) On the composition of intermediate hosts of cestodes, parasitic in the nine-spined stickleback.Angewandte Parasitologie 26, 147150.Google Scholar
Sysoev, A.V.(1987a) Seasonal dynamics of invasion of copepods with procercoids of cestodes in small lakes of Karelia. Angewandte Parasitologie 28, 191204.Google Scholar
Sysoev, A.V.(1987b) Copepods as intermediate hosts of Proteocephalus percae (Cestoda: Proteocephalidae) in some small lakes in Karelia Trudy GELAN 34, 105115.Google Scholar
Sysoev, A.V., Freze, V.I., Zitnan, R. & Hanzelová, V.(1988) Modus of chronecological substitution of hosts in polyhostal species of cestodes. Helminthologia 25, 287299.Google Scholar
Sysoev, A.V., Hanzelová, V., Yakushev, V.Y. & Freze, V.I.(1992) Some peculiarities of the process of infection transmission in cestodes of the genus Proteocephalus. Helminthologia 29, 1923.Google Scholar
Sysoev, A.V., Freze, V.I. & Andersen, K.I.(1994) On the morphology of procercoids of the genus Proteocephalus (Cestoda, Proteocephalidea)Parasitology Research 80, 245252.Google ScholarPubMed
Ubelaker, J.E.(1983) The morphology, development and evolution of tapeworm larvae. pp. 235296 in Arme, C. & Pappas, P.W. (Eds) Biology of the Eucestoda, vol. 1. London, Academic Press.Google Scholar
Valtonen, E.T. & Rintamäki, P.(1989) Occurrence of Proteocephalus percae and P. cernuae in the perch and ruff in northern Finland. Folia Parasitologica 36, 3342.Google ScholarPubMed
Vojtková, L. & Koubková, B.(1990) Helminth fauna of caddis-fly larvae (Megaloptera).Journal of the Faculty of Science, Masaryk University, Brno, Seria Biologia, 20, 494495. (In Czech.)Google Scholar
Wagner, E.D.(1953) A new species of Proteocephalus Weinland, 1858, (Cestoda), with notes on its life history Transactions of the American Microscopical Society 72, 364369.Google Scholar
Wagner, E.D.(1954) The life history of Proteocephalus tumidocollus Wagner, 1953 (Cestoda), in rainbow troutJournal of Parasitology 40, 489498.CrossRefGoogle ScholarPubMed
Wagner, O.(1917) Über den Entwicklungsgang und Bau einer Fischtaenie (Ichthyotaenia torulosus Batsch). Jena Zeitschrift für Naturwissenschaften 55, 166.Google Scholar
Wardle, R.A. & McLeod, J.A.(1952) The zoology of tapeworms. 780 pp. Minneapolis, University of Minnesota Press.Google Scholar
Wierzbicka, M.(1956) Wyniki sztucznego zarazenia Cyclops vicinus Ulj. larwami Proteocephalus percae (O.F. Müller, 1780). Acta Parasitologica Polonica 4, 89100.Google Scholar
Willemse, J.J.(1967) The host-parasite relation between fresh-water fishes and tapeworms of the genus Proteocephalus . Archives Néderlandaises de Zoologie 17, 289291.Google Scholar
Willemse, J.J.(1968) Proteocephalus filicollis (Rudolphi, 1802) and Proteocephalus ambiguus (Dujardin, 1845), two hitherto confused species of cestodes. Journal of Helminthology 42, 395410.Google Scholar
Willemse, J.J.(1969) The genus Proteocephalus in the Netherlands.Journal of Helminthology 43, 207222.CrossRefGoogle ScholarPubMed
Wootten, R.(1974) Studies on the life history and development of Proteocephalus percae (Müller) (Cestoda: Proteocephalidae)Journal of Helminthology 48, 269281.CrossRefGoogle ScholarPubMed
Yakushev, V.Y.(1984) Seasonal dynamics of the incidence of whitefish (Coregonus albula L.) invasion with a cestode Proteocephalus exiguus (Cestoda: Proteocephalidae) in Karelia. Helminthologia 21, 123130.Google Scholar
Yakushev, V.Y.(1985) Seasonal dynamics in the prevalence of Proteocephalus exiguus (Cestoda, Proteocephalidae) in Coregonus albula in Karelia.Parazitologiya 19, 95100. (In Russian.)Google Scholar
Yakushev, V.Y. & Chizhov, V.S.(1982) Attempted models of the process of distribution of Proteocephalus percae (Cestoidea: Proteocephalidae) in final host populations. Parazitologiya 16, 365376. (In Russian.)Google Scholar