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 | Parasitology | Cambridge Core (original) (raw)

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.

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, 63–122.Google Scholar

Baer, J. G. (1956). Parasitic helminths collected in West Greenland. Meddr Grønland, 124, 1–55.Google Scholar

Baer, J. G. (1961). Aspects ecologiques de la répartition des parasites chez leur hôtes. Wiad. parazyt. 7, 671–86.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, 463–539.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, 1–204.Google Scholar

Beneden, P. J. (1858). Mémoire sur les vers intestinaux. C. r. hebd. Séanc. Acad. Sci., Paris, 2, 1–376.Google Scholar

Beneden, P. J. (1870). Les poissons des côtes de Belgique, leurs parasites et leur commensaux. Mém. Acad. r. Sci. Lett. Belg. 38, 1–100.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), 1–588.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. 481–808, 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, 927–1173.Google Scholar

Cain, A. J. (1953). Geography, ecology and coexistence in relation to the biological definition of the species. Evolution, Lancaster, Pa., 7, 76–82.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, 1–131.Google Scholar

Cain, A. J. & Harrison, G. A. (1958). An analysis of the taxonomist's judgement of affinity. Proc. zool. Soc. Lond. 131, 85–98.CrossRefGoogle Scholar

Carus, J. V. (1863). Raderthiere, Würmer, Echinodermen, Coelenteraten und Protozoen. Handb. Zool. 2, 422–600.Google Scholar

Clark, R. S. (1922). Rays and skates (Raiae). 1. Egg capsules and young. J. mar. biol. Ass. U.K. 12, 577–643.Google Scholar

Coninck, L. de (1962). Problems of systematics and taxonomy in nematology today. Nematologica, 7, 1–7.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, 1–87.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, 1–819.Google Scholar

Diesing, K. M. (1863). Revision der Cephalocotyleen. Abtheilung: Paramecocotyleen. Sber. Akad. Wiss., Wien, 48, 200–345.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, 39–41.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, 141–416.Google Scholar

Gamble, F. W. (1896). The Cambridge Natural History. Vol. 2. Platyhelminthes and Mesozoa, pp. 1–96. 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, 81–104.Google Scholar

Hoyle, W. E. (1888). Tapeworms or Cestoda. Encycl. Brit. 9th ed., 23, 49–56.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. (1909–1910). Internal parasites of fishes from the Irish Sea. Lebouria idonea, Prosthecobothrium dujardinii (van Beneden), the genus Echeneibothrium. Proc. Trans. Lpool biol. Soc. 24, 78–99.Google Scholar

Johnstone, J. (1910–1911). Internal parasites and diseased conditions of fishes. Proc. Trans. Lpool biol. Soc. 25, 88–109.Google Scholar

Joyeux, Ch. & Baer, J. G. (1936). Cestodes. Faune Fr. 30, 1–613.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, 22–47.Google Scholar

Lebour, M. V. (1919). Feeding habits of some young fish. J. mar. biol. Ass. U.K. 12, 9–21.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. 453–511.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. 719–899.Google Scholar

Linton, E. (1897). Notes on larval cestode parasites of fishes. Proc. U.S. natn. Mus. 19, 787–824.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, 1–114.Google Scholar

Lonnberg, E. (1889). Bidrag till Kannedomen om I sverige forekommande Cestoder. Bih. K. svenska VetenskAkad. Handb. 14, 3–69.Google Scholar

Looss, A. (1892). Schmarotzertum in der Tierwelt. Zool. Vorträge, 10, 1–180.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, 1–41.Google Scholar

MacCallum, G. A. (1921). Studies in Helminthology. Zoopathologica, 1, 137–284.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. 45–51.Google Scholar

Mayr, E. (1957 a). Species concepts and definitions. In ‘The species problem'. Am. Ass. Adv. Sci. pp. 1–22.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. 7–14.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, 99–102.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, 695–707.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. 1–66.Google Scholar

Oerley, L. (1885). A Czápáknak és Rájáknak belférgei. Természetr. Füz. 9, 97–126.Google Scholar

Olsson, P. (1867). Entozoa iaktagna hos skandinaviska hafsfiskar. Acta Univ. lund. 3, 1–59.Google Scholar

Olsson, P. (1867–1868). Entozoa iaktagna hos skandinaviska hafsfiskar. Acta Univ. lund. 4, 1–64.Google Scholar

Olsson, P. (1893). Bidrag till Skandinaviens helminth fauna. II. K. Svenska VetenskAkad. Handl. 25, 1–41.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, 1–66.Google Scholar

Perrenoud, W. (1931). Recherches anatomiques et histologiques sur quelques cestodes de Sélaciens. Revue suisse Zool. 38, 469–555.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, 1–170.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, 263–305.Google Scholar

Rees, G. (1953). Some parasitic worms from fishes off the coast of Iceland. 1. Cestoda. Parasitology, 43, 4–14.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, 61–72.Google Scholar

Riser, N. (1955). Studies on cestode parasites of sharks and skates. J. Tenn. Acad. Sci. 30, 265–311.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. 43–96.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, 286–323.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, 1–34.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, 41–132.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, 187–376.Google Scholar

Wagener, G. R. (1854). Die Entwicklung der Cestoden. Nova Acta Acad. Caesar. Leop. Carol. 24, 1–91.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, 395–408.Google Scholar

Wilhelmi, R. W. (1940). Serological reactions and species specificity of some helminths. Biol. Bull. mar. biol. Lab., Woods Hole, 79, 64–90.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, 1–112.Google Scholar

Yamaguti, S. (1952). Studies on the helminth fauna of Japan. Part 49. Cestodes of Fishes. Acta Med. Okoyama, 8, 1–76.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, 41–50.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, 1–396.Google Scholar