Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-27T01:57:29.423Z Has data issue: false hasContentIssue false

The ecology, functional morphology and taxonomy of Echeneibothrium Beneden, 1849 (Cestoda: Tetraphyllidea), a revision of the genus and comments on Discobothrium Beneden, 1870, Pseudantho-bothrium Baer, 1956, and Phormobothrium Alexander, 1963

Published online by Cambridge University Press:  06 April 2009

H. Harford Williams
Affiliation:
Department of Zoology, University College of Wales, Aberystwyth*

Extract

Two new, nine little known species and nine unnamed ‘species’ of Echeneibothrium Beneden, 1850, have been investigated and observations have been made on the ‘related’ genera, Discobothrium Beneden, 1870, and Pseudanthobothrium Baer, 1956. Brief descriptions of the species are given, but a discussion of the history of each differs greatly from most previous accounts in that few or no synonyms have been listed for the species and in that nine forms are left unnamed; this approach differs greatly from that in a large number of taxonomic papers in helminthology. A detailed discussion of the reasons for adopting this procedure is, therefore, given. A provisional key to nineteen ‘species’ of Echeneibothrium is included. E. minutum sp.nov. closely resembles E. variabile var. exiguum of Euzet (1959), described in this paper as ‘Echeneibothrium sp. of R. clavata’, but occurs only in R. batis and differs in its very small size, in having only about ten proglottids, long peduncles to the bothridia and a myzorhynchus which remains evaginated in fixed specimens. It differs from E. demeusiae Euzet, 1959, mainly in the number of proglottids, testes and loculi. E. elongatum sp.nov. resembles E. dubium from which it differs in the length and form of the strobila, in having only six clearly visible loculi in each bothridium, about twenty testes and in that it occurs in R. circularis. It has, however, more characters in common with a species referred to in this paper as ‘Echeneibothrium sp. from Raja naevus’ and which possesses eight loculi. A list is given of twenty-seven species wrongly allocated by various authors to the genus Echeneibothrium. The comparative morphology of some species of the genus, their ecology and speculations on their life-histories, are described.

It is shown for the first time that Echeneibothrium from species of Raja caught off the British Isles, and presumably from rays of other localities, can be separated into two distinct biological groups. One group includes species which possess shallow open bothridia covering comparatively large areas of the host's mucosa, a variable myzorhynchus which may be either rudimentary or very large and spherical eggs laid singly or in capsules; these occur mainly in rays from shallow waters and in which the mucosa of the intestine lacks prominent villi. The other group includes species in which each bothridium possesses a small opening adapted for attachment to a single villus, the myzorhynchus is consistently cylindrical, the eggs have long polar filaments and the species occur in deep water rays with well-defined villi on the intestinal mucosa. Studies on variation in the form of the eggs in different species of Echeneibothrium in relation to the behaviour and feeding habits of the various host-species suggest that the eggs are eaten by arthropods which are most likely to form part of the diet of the final host. A general trend towards an increase in the complexity of the bothridium and a decrease in the size of the myzorhynchus in Echeneibothrium is thought to be of considerable advantage to the species and an indication that Rhinebothrium, which is restricted to the Myliobatoidea, has evolved from a form like Echeneibothrium which is restricted to the Rajoidea. This supports the view that the Myliobatoidea have evolved from the Rajoidea. The results from this study of Echeneibothrium illustrate the following general rule which can be applied to the Tetraphyllidea, namely, those species which are abundant in any given host are very well adapted for attachment to the host's gut and cause little, if any, damage while rare species are often highly pathogenic.

This work would not have been possible without generous financial aid from the Department of Scientific and Industrial Research and various kinds of other aid and encouragement from a number of persons, in particular Dr Gwendolen Rees.

It was begun in 1958 at the University College of Wales, Aberystwyth, the British Museum (Natural History), University of Montpellier, France, University of Neuchatel, Switzerland, the Plymouth Marine Laboratory and the Aberdeen Marine Laboratory during my tenure of a D.S.I.R. Fellowship. I wish to record my gratitude to Dr Rees who has also suggested improvements to the manuscript and to the following persons: the late Professor T. A. Stephenson, F.R.S., Dr E. E. Watkin, Mr S. Prudhoe, Dr L. Euzet, Professor Jean G. Baer, The Director, Dr F. S. Russell and Staff, in particular Mr J. Green and Mr A. Mattacola, of the Plymouth Marine Laboratory, and the Director and staff, in particular Dr B. B. Rae and Dr Z. Kabata, of the Aberdeen Marine Laboratory.

The work was later continued at the University College, Cardiff, and I am most grateful to Professor James Brough for providing excellent research facilities and to Mr W. O'Grady for technical assistance.

At the Bureau of Helminthology, St Albans, much encouragement from Professor R. T. Leiper, C.M.G., F.R.S., enabled me to put the work together while having free access to his invaluable collection of books and reprints on helminths; it became unnecessary to search elsewhere for the literature. Mr G. Dimmock gave technical assistance for which I am most grateful.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1966

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

Alexander, C. G. (1963). Tetraphyllidean and Diphyllidean Cestodes of New Zealand Selachians. Trans. R. Soc. N.Z. 3, 117–42.Google Scholar
Anantaraman, S. (1963). Larval cestodes in marine invertebrates and fishes with a discussion of the life cycles of the Tetraphyllidea and the Trypanorhyncha. Z. ParasitKde, 23, 309–14.CrossRefGoogle ScholarPubMed
Andrew, W. (1959). Textbook of Comparative Histology, 652 pp. London: Oxford University Press.Google Scholar
Baer, J. G. (1948). Contributions a l'étude des cestodes de selaciens Institut de Zoologie Universite de Neuchâtel. Bull. Soc. neuchâtel. Sci. nat. 71, 63122.Google Scholar
Baer, J. G. (1956). Parasitic helminths collected in West Greenland. Meddr Grønland, 124, 155.Google Scholar
Baer, J. G. (1961). Aspects ecologiques de la répartition des parasites chez leur hôtes. Wiad. parazyt. 7, 671–86.Google Scholar
Baer, J. G. (1962). Cestoda. Zoology, Iceland, 2, 163.Google Scholar
Baylis, H. A. (1939). Further records of parasitic worms from British vertebrates. Ann. Mag. nat. Hist. 4, 473–98.CrossRefGoogle Scholar
Baylis, H. A. (1947). Some roundworms and flatworms from the West Indies and Surinam. II. Cestodes. J. Linn. Soc. 41, 407–13.Google Scholar
Baylis, H. A. & Jones, E. I. (1933). Some records of parasitic worms from marine fishes at Plymouth. J. mar. biol. Ass. U.K. 18, 627–34.Google Scholar
Beauchamp, P. M. de (1905). Études sur les cestodes des Sélaciens. Archs Parasit. 9, 463539.Google Scholar
Beneden, P. J. (1849). Les helminthes cestoides, considérés sous le rapport de leurs métamorphoses, de leur composition anatomique et de leur classification et mention de quelques espèces nouvelles de nos poissons plagiostomes. Bull. Acad. r. Belg. Cl. Sci. 16, 269–82.Google Scholar
Beneden, P. J. (1850 a). Les helminthes cestoides, considérés sous le rapport de leurs métamorphoses, de leur composition anatomique et de leur classification et mention de quelques espèces nouvelles de nos poissons plagiostomes. [Report]. Bull. Acad. r. Belg. Cl. Sci. 17, 102–8.Google Scholar
Beneden, P. J. (1850 b). Recherches sur la faune littorale de Belgique; Les vers cestoides considérés sous le rapport physiologique, embryogénique et zooclassique. Mém. Acad. r. Sci. Lett. Belg. 25, 1204.Google Scholar
Beneden, P. J. (1858). Mémoire sur les vers intestinaux. C. r. hebd. Séanc. Acad. Sci., Paris, 2, 1376.Google Scholar
Beneden, P. J. (1870). Les poissons des côtes de Belgique, leurs parasites et leur commensaux. Mém. Acad. r. Sci. Lett. Belg. 38, 1100.Google Scholar
Bigelow, H. B. & Schroeder, W. C. (1953). Fishes of the Western North Atlantic. Sawfishes, guitarfishes, skates and rays. Mem. Sears Fdn mar. Res. 1 (2), 1588.Google Scholar
Blanchard, R. A. E. (1888). Protozoaires, histoire de l'œuf, coelentérés, échinodermes, vers (aneuriens, plathelminthes, némathelminthes). In Traité de zoologie médicale, vol. 5, pp. 481808, Paris.Google Scholar
Borcea, L. (1934). Note préliminaire sur les cestodes des Elasmobranches ou Sélaciens de la Mer Noire. Annls scient. Univ. Jassy, 19, 345–69.Google Scholar
Braun, M. G. C. C. (1894-1900). Vermes. Bronn's Kl. Ordn. Tierreichs, 4, 9271173.Google Scholar
Cain, A. J. (1953). Geography, ecology and coexistence in relation to the biological definition of the species. Evolution, Lancaster, Pa., 7, 7682.Google Scholar
Cain, A. J. (1954). Animal Species and their Evolution, 190 pp. London: Hutchinsons University Library.Google Scholar
Cain, A. J. (1959 a). The post Linnaean development of taxonomy. Proc. Linn. Soc. Lond. 170, 234–44.CrossRefGoogle Scholar
Cain, A. J. (1959 b). Function and taxonomic importance. Systematics Association Publication, no. 3, 1131.Google Scholar
Cain, A. J. & Harrison, G. A. (1958). An analysis of the taxonomist's judgement of affinity. Proc. zool. Soc. Lond. 131, 8598.CrossRefGoogle Scholar
Carus, J. V. (1863). Raderthiere, Würmer, Echinodermen, Coelenteraten und Protozoen. Handb. Zool. 2, 422600.Google Scholar
Clark, R. S. (1922). Rays and skates (Raiae). 1. Egg capsules and young. J. mar. biol. Ass. U.K. 12, 577643.Google Scholar
Coninck, L. de (1962). Problems of systematics and taxonomy in nematology today. Nematologica, 7, 17.Google Scholar
Deblock, S., Rosé, F., Broussart, J., Capron, A. & Brygoo, E. R. (1962). Miscellanea helminthologica madagascariensia. Cestodes de Madagascar et des îles voisines. Archs Inst. Pasteur Madagascar, 31, 187.Google Scholar
Deslongchamps, E. E. (1824). Histoire naturelle des zoophytes, ou animaux rayonnés, faisant suite à l'histoire naturelle des vers de Brugière. Encycl. Methodique Hist. Nat. 2, 1819.Google Scholar
Diesing, K. M. (1863). Revision der Cephalocotyleen. Abtheilung: Paramecocotyleen. Sber. Akad. Wiss., Wien, 48, 200345.Google Scholar
Dollfus, R. Ph. (1923). Énumération des cestodes du plancton et des invertébrés marins. 2. Mollusques céphalopodes et Crustacés. Annls Parasit. hum. comp. 1, 363–94.CrossRefGoogle Scholar
Dollfus, R. Ph. (1931). Nouvel addendum à mon ‘Énumeration des cestodes du plancton et des invertébrés marins'. Annls Parasit. hum. comp. 9, 552–60.Google Scholar
Douglas, L. T. (1963). The development of organ systems in nematotaeniid cestodes. III. Gametogenesis and embryonic development in Baerietta diana and Distoichometra kozloffi. J. Parasit. 49, 530–57.Google Scholar
Erasmus, D. A. (1962). Studies on the adult and metacercaria of Holostephanus luhei Szidat, 1936. Parasitology, 52, 353–74.Google Scholar
Euzet, L. (1953). Cestodes tetraphyllides nouveaux ou peu connus de Dasyatis pastinaca (L.). Annls Parasit. hum. comp. 28, 339–51.Google Scholar
Euzet, L. (1956). Une espèce nouvelle d'Echeneibothrium Van Ben. 1850. Bull. Soc. neuchâtel. Sci. nat. 79, 3941.Google Scholar
Euzet, L. (1959). Recherches sur les cestodes Tétraphyllides des Sélaciens des côtes de France. Thès. Fac. Sci. Université Montpellier, 263 pp.Google Scholar
Ewing, S. A. & Todd, A. C. (1961). Association among members of the genus Metastrongylus Molin, 1861 (Nematoda: Metastrongylidae). Am. J. vet. Res. 22, 1077–80.Google Scholar
Fuhrmann, O. (1931). Dritte Klasse des Cladus Plathelminthes: Cestoidea. Handb. Zool. 2, 141416.Google Scholar
Gamble, F. W. (1896). The Cambridge Natural History. Vol. 2. Platyhelminthes and Mesozoa, pp. 196. London: Macmillan and Co. Ltd.Google Scholar
Hart, J. F. (1936). Cestoda from fishes of Puget Sound. III. Phyllobothrioidea. Trans. Am. microsc. Soc. 55, 488–96.Google Scholar
Heller, A. F. (1949). Parasites of cod and other marine fish from the Baie de Chaleur region. Can. J. Res. 27, 243–64.Google Scholar
Hickman, J. L. (1963). The biology of Oochoristica vacuolata Hickman (Cestoda). Pap. Proc. R. Soc. Tasm. 97, 81104.Google Scholar
Hoyle, W. E. (1888). Tapeworms or Cestoda. Encycl. Brit. 9th ed., 23, 4956.Google Scholar
Hunter, W. S. (1950). The nemertean, Cerebratulus lacteus, as an intermediate host for cestode larvae. J. Parasit. 36, 496.CrossRefGoogle ScholarPubMed
Huxley, J. S. (1940). The New Systematics, 583 pp. Oxford: Clarendon Press.Google Scholar
Huxley, J. S. (1942). Evolution: The Modern Synthesis, 645 pp. London: Allen and Unwin.Google Scholar
Hyman, L. H. (1951). The Invertebrates. Vol. n. Platyhelminthes and Rhynchocoela, 550 pp. New York and London: McGraw-Hill Book Co. Inc.Google Scholar
Jackson, W. H. (1888). Forms of Animal Life. A Manual of Comparative Anatomy with Descriptions of Selected Types, 937 pp. Oxford.Google Scholar
Jarecka, L. (1961). Morphological adaptations of tapeworm eggs and their importance in the life cycles. Acta parasit. pol. 9, 409–26.Google Scholar
Johnstone, J. (1906). Internal parasites and diseased conditions of fishes. Proc. Trans. Lpool biol. Soc. 20, 151–85.Google Scholar
Johnstone, J. (19091910). Internal parasites of fishes from the Irish Sea. Lebouria idonea, Prosthecobothrium dujardinii (van Beneden), the genus Echeneibothrium. Proc. Trans. Lpool biol. Soc. 24, 7899.Google Scholar
Johnstone, J. (19101911). Internal parasites and diseased conditions of fishes. Proc. Trans. Lpool biol. Soc. 25, 88109.Google Scholar
Joyeux, Ch. & Baer, J. G. (1936). Cestodes. Faune Fr. 30, 1613.Google Scholar
Joyeux, Ch. & Baer, J. G. (1961). Classe des Cestodes. In Traité de Zoologie, Anatomie, Systematique, Biologie.4. Plathelminthes, Mesozaires, Acanthocéphales, Némertiens, 944 pp. Paris: Masson et Cie.Google Scholar
Kassai, T. & Mahunka, S. (1964). Vizagálatok a monieziák köztigazdáiróil. Magy. Állatorv. Lap. 19, 531–8.Google Scholar
Khambata, F. S. & Bal, D. V. (1951). Five new species of cestodes from marine fishes of Bombay. [Abstract.] Proc. Indian Sci. Congr.Google Scholar
Kholodkovskii, N. A. (1899). Meditsinskaya zoologija; sostavil po lektsiyam P. Berkos, 355 pp. Petersburg.Google Scholar
Lebour, M. V. (1918). The food of post larval fish. J. mar. biol. Ass. U.K. 12, 2247.Google Scholar
Lebour, M. V. (1919). Feeding habits of some young fish. J. mar. biol. Ass. U.K. 12, 921.CrossRefGoogle Scholar
Lee, D. L. (1962). Studies on the function of the pseudosuckers and holdfast organ of Diplostomum phoxini Faust (Strigeida, Trematoda). Parasitology, 52, 103–12.Google Scholar
Leuckart, K. G. F. R. (1886). The Parasites of Man, and the Diseases which Proceed them, 771 pp. Edinburgh.Google Scholar
Linstow, O. F. B. von (1903). Entozoa des zoologischen Museums der Kaiserlichen Akademie der Wissenschaften zu St Petersburg. Ezheg. zool. Muz. 8, 265–94.Google Scholar
Linton, E. (1889). Notes on entozoa of marine fishes of New England with descriptions of several new species. Rep. U.S. Commnr Fish. pp. 453511.Google Scholar
Linton, E. (1890). Notes on Entozoa of marine fishes of New England with descriptions of several new species. Part II. Rep. U.S. Commnr Fish. pp. 719899.Google Scholar
Linton, E. (1897). Notes on larval cestode parasites of fishes. Proc. U.S. natn. Mus. 19, 787824.Google Scholar
Linton, E. (1901). Parasites of fishes of the Woods Hole region. Bull. U.S. Fish Commn. 19, 405–92.Google Scholar
Linton, E. (1924). Notes on cestode parasites of sharks and skates. Proc. U.S. natn. Mus. 64, 1114.Google Scholar
Lonnberg, E. (1889). Bidrag till Kannedomen om I sverige forekommande Cestoder. Bih. K. svenska VetenskAkad. Handb. 14, 369.Google Scholar
Looss, A. (1892). Schmarotzertum in der Tierwelt. Zool. Vorträge, 10, 1180.Google Scholar
Lopez-Neyra, C. R. & Diaz-Ungria, C. (1958). Cestodes de Venezuela. V. Cestodes de vertebrados Venezolanos. (Segunda Noya.) Noved. cient. Mus. Hist. nat. La Salle, 23, 141.Google Scholar
MacCallum, G. A. (1921). Studies in Helminthology. Zoopathologica, 1, 137284.Google Scholar
Mayr, E. (1942). Systematics and the Origin of Species, 334 pp. New York: Columbia University Press.Google Scholar
Mayr, E. (1955). Systematics and modes of speciation in ‘Biological Systematics’. Proc. 16th A. Biol. Coll. Ore. St. Coll. pp. 4551.Google Scholar
Mayr, E. (1957 a). Species concepts and definitions. In ‘The species problem'. Am. Ass. Adv. Sci. pp. 122.Google Scholar
Mayr, E. (1957 b). Evolutionary aspects of host specificity among parasites of vertebrates. In 1st Symp. on Host Specificity among Parasites of Vertebrates. University of Neuchâtel. pp. 714.Google Scholar
Mayr, E. (1959). Isolation as an evolutionary factor. Proc. Am. phil. Soc. 103, 221–30.Google Scholar
Mayr, E., Linsley, E. & Usinger, R. (1953). Methods and Principles of Systematic Zoology, 328 pp. New York and London: McGraw-Hill Book Co. Inc.Google Scholar
Mettrick, D. F. (1961). Contributions to the helminth fauna of Central Africa. III. Host specificity in the genus Inermicapsifer Janicki, 1910. Proc. Trans. Rhod. scient. Ass. 49, 99102.Google Scholar
Mettrick, D. F. (1963). A statistical analysis of the morphological variation observed between populations of Zonorchis petiolatum (Railliet, 1900) (Trematoda: Dicrocoeliidae) from different hosts and localities. J. Parasit. 49, 745–51.Google Scholar
Michajlow, W. (1961). Biological problems of ‘parasite–host’ relations. Wiad. parazyt. 7, 695707.Google ScholarPubMed
Monticelli, F. S. (1890). Elenco degli elminti studiati a Wimereux nella primavera del 1889. Bull. scient. Fr. Belg. 22, 418–44.Google Scholar
Norman, J. R. (1935). List of British Vertebrates. Brit. Mus. Nat. Hist. pp. 166.Google Scholar
Oerley, L. (1885). A Czápáknak és Rájáknak belférgei. Természetr. Füz. 9, 97126.Google Scholar
Olsson, P. (1867). Entozoa iaktagna hos skandinaviska hafsfiskar. Acta Univ. lund. 3, 159.Google Scholar
Olsson, P. (18671868). Entozoa iaktagna hos skandinaviska hafsfiskar. Acta Univ. lund. 4, 164.Google Scholar
Olsson, P. (1893). Bidrag till Skandinaviens helminth fauna. II. K. Svenska VetenskAkad. Handl. 25, 141.Google Scholar
Pantin, C. F. A. (1954). The recognition of species. Sci. Prog., Lond. 168, 587–98.Google Scholar
Paperna, I. (1964). The metazoan parasite fauna of Israel inland water fishes. Bamidgeh. 16, 166.Google Scholar
Perrenoud, W. (1931). Recherches anatomiques et histologiques sur quelques cestodes de Sélaciens. Revue suisse Zool. 38, 469555.Google Scholar
Petter, A. J. (1963). Equilibre des especes dans les populations de nematodes parasites du colon des tortues terrestres. C. r. Séanc. Acad. Sci., Paris, 257, 2152–4.Google Scholar
Polyanski, Y. I. (1955). Contribution to parasitology of fishes of the northern seas of the U.S.S.R. Fish parasites in the Barents Sea. Trudy zool. Inst., Leningr., 19, 1170.Google Scholar
Polyanski, Y. I. (1957). Some problems of fish parasitology in the Barents Sea. Trudy murmansk. biol. Sta. 3, 175–83.Google Scholar
Read, C. P. & Simmons, J. W., Jr. (1963). Biochemistry and physiology of tapeworms. Physiol. Rev. 43, 263305.Google Scholar
Rees, G. (1953). Some parasitic worms from fishes off the coast of Iceland. 1. Cestoda. Parasitology, 43, 414.Google Scholar
Rees, G. & Llewellyn, J. (1941). A record of the trematode and cestode parasites of fishes from the Porcupine Bank, Irish Atlantic Slope and Irish Sea. Parasitology, 33, 390–96.Google Scholar
Reichenbach-Klinke, H. H. (1956). Die Entwicklung der Larven bei der Bandwurmordnung Tetraphyllidea Braun 1900. Abh. braunschw. wiss. Ges. 8, 6172.Google Scholar
Riser, N. (1955). Studies on cestode parasites of sharks and skates. J. Tenn. Acad. Sci. 30, 265311.Google Scholar
Rudolphi, C. A. (1819). Entozoorum Synopsis cui accedunt mantissa duplex et indices locupletissimi, 811 pp. Berolini.Google Scholar
Sandars, D. F. (1957). Redescription of some cestodes from marsupials. I. Taeniidae. Ann. trop. Med. Parasit. 51, 317–29.Google Scholar
Schad, G. A. (1962). Gause's hypothesis in relation to the oxyuroid populations of Testudo graeca. J. Parasit. 48, 36–7.Google Scholar
Schad, G. A. (1963). Niche diversification in a parasitic species flock. Nature, Lond., 198, 404–6.Google Scholar
Shipley, A. E. & Hornell, J. (1906). Report on the Cestode and Nematode parasites from the marine fishes of Ceylon. Ceylon Pearl Oyster Report, pp. 4396.Google Scholar
Siebold, C. T. E. (1854). Anatomy of the Invertebrata, 470 pp. London and Boston.Google Scholar
Simpson, G. F. (1943). Tempo and Mode in Evolution, 237 pp. New York: Columbia University Press.Google Scholar
Simpson, G. F. (1961). Principles of Animal Taxonomy, 247 pp. London: Oxford University Press.Google Scholar
Sindermann, C. J. (1963). Immunogenetic studies of elasmobranch fishes. Int. Congr. Zool., Washington, 1963, vol. 2, pp. 210.Google Scholar
Smyth, J. D. (1962). Lysis of Echinococcus granulosus by surface active agents in bile and the role of this phenomenon in the determination of host specificity in helminths. Proc. R. Soc. B, 156, 553–72.Google Scholar
Smyth, J. D. (1963 a). Secretory activity by the scolex of Echinococcus granulosus in vitro. Nature, Lond., 199, 402.CrossRefGoogle Scholar
Smyth, J. D. (1963 b). The biology of cestode life cycles. Tech. Commun. Commonw. Bur. Helminth. 38 pp.Google Scholar
Smyth, J. D. & Clegg, J. A. (1959). Egg-shell formation in trematodes and cestodes. Expl Parasit. 8, 286323.Google Scholar
Southwell, T. (1925). A Monograph on the Tetraphyllidea with Notes on Related Cestodes, 386 pp. Mem. Lpool Sch. trop. Med. Liverpool University Press.Google Scholar
Southwell, T. (1930). Cestoda. Vol. 1. The Fauna of British India including Ceylon and Burma, 391 pp. London: Taylor and Francis.Google Scholar
Steven, G. A. (1932). Rays and skates of Devon and Cornwall. II. A study of the fishery with notes on the occurrence, migrations and habits of the species. J. mar. biol. Ass. U.K. 18, 134.Google Scholar
Stossich, M. (1898). Saggio di una fauna elmintologica di Trieste e provincie contermini. Program. Civ. Scuola R. Sup. Trieste, 19, 162 pp.Google Scholar
Subhapradha, C. K. (1955). Cestode parasites of fishes of Madras coast. Indian J. Helminth. 7, 41132.Google Scholar
Subramaniam, K. (1939). On a new species of Echeneibothrium from Rhinobatus granulatus. Rec. Indian Mus. 42, 457–64.Google Scholar
Tseng, S. (1933). Study on some cestodes from fishes. J. Sci. natn. Univ. Shantung, 2, 21.Google Scholar
Vaullegeard, A. (1899). Recherches sur les tetrarhynques. Mém. Soc. linn. Normandie, 19, 187376.Google Scholar
Wagener, G. R. (1854). Die Entwicklung der Cestoden. Nova Acta Acad. Caesar. Leop. Carol. 24, 191.Google Scholar
Wardle, R. A. & McLeod, J. A. (1952). The Zoology of Tapeworms, 780 pp. Minneapolis: University of Minnesota Press.Google Scholar
Wedl, C. (1855). Zur Ovologie und Embryologie der Helminthen. Sber. Akad. Wiss. Wien, 16, 395408.Google Scholar
Wilhelmi, R. W. (1940). Serological reactions and species specificity of some helminths. Biol. Bull. mar. biol. Lab., Woods Hole, 79, 6490.Google Scholar
Williams, H. H. (1958 a). Some Tetraphyllidea (Cestoda) from the Liverpool School of Tropical Medicine. Rev. suisse Zool. 65, 867–78.Google Scholar
Williams, H. H. (1958 b). Some Phyllobothriidae (Cestoda: Tetraphyllidea) of elasmobranchs from the western seaboard of the British Isles. Ann. Mag. nat. Hist. 1, 113–36.Google Scholar
Williams, H. H. (1959). A list of parasitic worms, including 22 new records, from marine fishes caught off the British Isles. Ann. Mag. nat. Hist. 2, 705–15.Google Scholar
Williams, H. H. (1960). The intestine in members of the genus Raja and host specificity in the Tetraphyllidea. Nature, Lond., 188, 514–16.Google Scholar
Williams, H. H. (1961). Observations on Echeneibothrium maculatum (Cestoda: Tetraphyllidea). J. mar. biol. Ass. U.K. 41, 631–52.Google Scholar
Williams, H. H. (1963). Observations on Echeneibothrium (Cestoda: Tetraphyllidea) from various species of Raja. Parasitology, 53, 9p.Google Scholar
Woodland, W. N. F. (1927). A revised classification of tetraphyllidean Cestoda, with descriptions of some Phyllobothriidae from Plymouth. Proc. zool. Soc. Lond. pp. 519–42.Google Scholar
Yamaguti, S. (1934). Studies on the helminth fauna of Japan. Part 4. Cestodes of fishes. Jap. J. Zool. 6, 1112.Google Scholar
Yamaguti, S. (1952). Studies on the helminth fauna of Japan. Part 49. Cestodes of Fishes. Acta Med. Okoyama, 8, 176.Google Scholar
Yamaguti, S. (1959). Systema Helminthum. 2. The Cestodes of Vertebrates, 860 pp. London: Interscience Publishers Ltd.Google Scholar
Yamaguti, S. (1960). Studies on the helminth fauna of Japan, Part 56. Cestodes of Fishes. III. Publs Seto mar. biol. Lab. 8, 4150.Google Scholar
Young, R. T. (1954). Cestodes of sharks and rays in Southern California. Proc. helminth. Soc. Wash. 21, 106–12.Google Scholar
Young, R. T. (1955). Two new species of Echeneibothrium from the stingray Urobatis halleri. Trans. Am. microsc. Soc. 74, 232–4.Google Scholar
Young, R. T. (1956). A review of the cestode genus Echeneibothrium. Proc. Wash. Acad. Sci. 46, 256–65.Google Scholar
Zschokke, F. (1888). Recherches sur la structure anatomique et histologique des Cestodes. Mém. Inst. natn. génev. 17, 1396.Google Scholar