zyxwvuts zyxwvuts zyxwvutsrqpon zyxwvut zyxwvut J . Fish Biol. (1 987) 31,5 17-543 A key to the species of cestodes (tapeworms) parasitic in British and Irish freshwater fishes zyxwv J. C. CHUBB*, D. W. POOLANDC. J. VELTKAMP Deportment of’Zoology, University of’liverpool, P . 0 .Box 147, Liverpool L69 3BX. England (Received 22 January 1987, Accepted 20 February 1987) Methods for the collection, fixation. preservation and examination of the cestodes parasitic in British freshwater fishes are described. An illustrated key to the species is provided, with the exception of the members of the genus Proreoccphalus. for which the information is tabulated. I. INTRODUCTION Thirty-three species of cestodes from six orders have been recorded as adults or larvae from freshwater fishes in the British Isles. Two of these identifications were regarded as dubious by the respective authors (Caryophyllaeus jimbriceps, Kennedy, 1974; Proteocephalus parallacticus, Arme & Ingham, 1972). We include these two species in the key, although we have no additional evidence to confirm the determinations. Those species of cestodes found in marine fishes which migrate into brackish or fresh waters are included in the key, except for ‘ Scolex pleuronectis ’ (see Discussion). Identification of the cestodes of freshwater fishes in the British Isles is generally a straightforward procedure. However, it has been made complicated and timeconsuming by the need to use foreign texts which contain species not occurring in the British Isles (e.g. Bykhovskaya-Pavlovskaya et al., 1962). In addition, many of the line drawings of the scolices of the cestodes in existing keys lack realism, which can impede accurate identification. The aim of the present paper is to remedy this by providing scanning electron microscope (SEM)photographs of a representative individual of each species and a checklist of the species known to occur in the British Isles. In most instances the cestodes can be identified by scolex morphology together with knowledge of the species of host. Where additional morphological information is necessary, as for example to separate Bathybothrium rectangulum from Bothriocephalus acheilognathi, we have provided this. However, we have not attempted to include comprehensive morphological descriptions of each species. Except in a few instances, we have avoided reference to size of the cestodes, as this is influenced by the age and dimensions of the host (Davydov, 1978), the species of host (Read & Voge, 1954; Freze, 1977), the intensity of infection (Pavlovski & Gnezdilov, 1949) and the state of contraction or relaxation of the parasite (Pool & Chubb, 1985). Where taxonomic problems are unresolved, or where we suspect they may exist, they are indicated at the relevant point in the discussion. We have adopted a zyxw *For correspondence. 517 0022-1 I12/87/010517+27$03.00/0 0 1987 The Fisheries Society of the British Isles 518 zyxwvutsrq zyxwv zyxwvutsrq J . C . CHUBB ET A L . dichotomous format for the key, with the exception of the species within the genus Profeocephalus, where the information for differentiation of the species is presented in tabular form. zyxw 11. MATERIALS AND METHODS PREPARATION OF MATERIALS Whenever possible, fishes should be examined freshly killed. At autopsy the contents of the stomach, pyloric caeca and intestine lumen should be examined for adult cestodes. Larval stages may occur free in the body cavities or be encapsulated within the tissue of a wide variety of organs of the fish. The scolex and anterior parts of the strobila of living cestodes are often highly mobile. Differing fixation procedures can, as a consequence, induce a high degree of variation in form (Pool & Chubb, 1985). It is, therefore, important to adopt a standardized procedure for relaxation and fixation of worms in order to obtain consistent results. We recommend that the living adult cestodes should be removed from the alimentary tract, relaxed in distilled water at 10" C for either 60 min or until movement has ceased, and then fixed in 4% neutral buffered formaldehyde solution for at least 24 h. In this way, extremes ofcontraction or relaxation are avoided. Larval cestodes are treated in a similar manner after they have been freed from host tissues; relaxation may take a much longer time than for adult worms, but a close watch should be kept on the specimens, as excessive relaxation may result in the partial sloughing of the tegument. EXAMINATION OF T H E SCOLEX Using a binocular microscope, the three-dimensional structure of the scolex can be seen in all but the smallest species. Better detail can be obtained, if necessary, using an SEM, although this will rarely be essential for identification. In this key, SEM photographs are presented because they demonstrate a degree of realism unobtainable by any other method. The specimens were fixed as described above. They were then washed in distilled water, dehydrated in an ethanol series, critical-pointdried in carbon dioxide using a Polaron E3000, and sputter-coated in a Polaron E5 I00 using 60% gold/palladium. They were viewed in a Philips 501B SEM at 7.2 kV. Subsequent decoating of specimens can be achieved in acetone if necessary. zyx EXAMINATION OF T H E STROBILA Differentiation of Bathybothrium rectangulum and Bothriocephalus acheilognathi is facilitated by examination of the arrangement of the genitalia within the proglottis. These two species are readily separated by the position of the vitelline glands, which are visible in material fixed in neutral buffered formaldehyde as described above. 1'0facilitate examination, whole worms or pieces of strobila are transferred sequentially from fixative to distilled water, 30%, 50% and 70% ethanol, and finally to a mixture of 3 parts 70% ethanol to 1 part pure glycerine. The ethanol is allowed to evaporate, leaving the cleared materials in glycerine. If required, mounts can be made in glycerine jelly and ringed to provide reasonable permanence. To demonstrate fuller details of cestode genitalia in a whole mount, for examination using optical microscopy, the technique of Schnur (1969) is recommended. This relatively straightforward procedure, using methylene blue stain, has been found to be effective for a wide variety of cestodes. It is especially useful for members of the genus Proteocephalus, where the size and position of the cirrus sac and the numbers of testes are important for identification. 111. CHECK LIST OF SPECIES OF CESTODES KNOWN TO OCCUR IN BRITAIN AND IRELAND The species are arranged alphabetically within each order. An asterisk indicates that the author who found this species in the British Isles expressed doubts concerning identification. Species found as larval stages in fishes are indicated as such; zyxwvutsr zyxw zyxw zyxw zyxwvuts A K E Y TO THE SPECIES OF CESTODES 519 all other species occur as adults in fishes. Species of marine origin, but found in fishes in fresh waters, are noted. Order Caryophyllidea van Beneden in Carus, 1863 Archigetes sieboldi Leuckart, 1878 Caryophyllaeidesjennica (Schneider, 1902) Caryophyllueus laticeps (Pallas, 1781) * Carq’ophyllaeus,fimbriceps Annenkova-Khlopina, 1919 Order Spathebothriidea Wardle and McLeod, 1952 Cyathocephalus truncatus (Pallas, 1781) Order Trypanorhyncha Diesing, 1863 Heputoxylon squali (Martin, 1797), larval, marine origin Order Pseudophyllidea Carus, 1863 Buthybothrium rectangulum (Bloch, 1782) Bothriocephulus acheilognathi Yamaguti, 1934 B. cluuiceps (Goeze, 1782) Diphyllohothrium dentriticuni (Nitzsch, 1824), larval D. ditremum (Creplin, 1825), larval D. latum (Linnaeus, 1758), larval *D. vogeli Kuhlow, 1953, larval Eubothrium crassum (Bloch, 1779) E. frugilis (Rudolphi, 1802), marine origin E. suluelini (Schrank, 1790) Ligula intestinalis (Linnaeus, 1758), larval Schistocephalus pungitii Dubinina, 1959, larval S. solidus (Miiller, 1776), larval Triaenophorus nodulosus (Pallas, 178I ) , larval and adult Order Tetraphyllidea Carus, 1863 ‘ Scolex pleuronectis ’ Muller, 1788, larval, marine origin: see Discussion Order Proteocephalidea Mola, 1928 Proteocephalus ambiguus (Dujardin, 1845) P. cernua (Gmelin, 1790) P. exiguus La Rue, 191 1 P.jlicollis (Rudolphi, 1802) P. macrocephalus (Creplin, 1825) P. neglectus La Rue 1911 P. ocellatus (Rudolphi, 1802) [nec P. percae (Muller, 1780)] P. osculatus (Goeze, 1782) * P. parallacticus MacLulich, 1943 P. pollanicola Gresson, 1952 P. sagittus (Grimm, 1872) P. torulosus (Batsch, 1786) 520 zyxwvuts zyxwvut zyxw J. C . CHUBB E T A L . Order Cyclophyllidea van Beneden in Braun, 1900 Valipora cumpyluncristrota (Wedl, 1855), larval [ = Dilepis unilateralis (Krabbe, 1869)] 1V. KEY TO THE SPECIES OF CESTODES PARASITIC IN BRITISH AND IRISH FRESHWATER FISHES 1. Parasitic in body cavity, viscera (other than lumen of intestine) or musculature. Genitalia, if present, not mature Larval cestodes 2 Parasitic in lumen of intestine (or pyloric caeca, if present). Genitalia usually evident unless worms juvenile. In gravid specimens eggs usually clearly visible Adult cestodes 11 zyxwvu LARVAL CESTODES 2. Larvae less than 1 mm long. Scolex with four suckers and an armed rostellum of two circles of hooks, 10 large (20-29 pm long) and 10 small (9-10 pm long) Valipora campylancristrota (Figs 1,2). Cysticercoid (cercoscolex of Jarecka, 1970) in lumen of the gall bladder of carp Cyprinus carpio L. (Dearsley et al., 1982). Rostellum often retracted (Fig. 2). Adult tapeworms in intestine of heron Ardea cinerea L. Probably widespread, despite few British records so far. Larvae more than 1 mm long, scolex without four suckers or an armed rostellum 3 3. Found free in body cavity or entangled with alimentary viscera. Scolex 4 domed, but hardly visible at low magnifications ( x 10) Found encapsulated in or attached to alimentary viscera or in musculature. Scolex not domed, usually readily visible at low magnifications ( x 10) 6 4. Scolex dome clearly bisected by a furrow when viewed apically at high magnification ( x 400). Annulation ( =segmentation) as broken circles, not concurrent with proglottis rudiments Ligula intestinalis (Figs 3,4). Plerocercoid parasitic in body cavity of cyprinid fishes. Copepods are first intermediate hosts, piscivorous birds or mammals definitive hosts. Widespread throughout British Isles, often locally abundant but sporadic in occurrence. Scolex dome not bisected when viewed apically. Annulation as complete circles, concurrent with proglottis rudiments 5 5 . Shoulder of first annulation curved along its length (see three arrows in Fig. 6). Parasite of Pungitius pungitius Schistocephalus pungitii (Figs 5 , 6). Plerocercoid in body cavity of ten-spined stickleback, P. pungitius (L.). Copepods are first intermediate hosts, piscivorous birds or mammals definitive hosts. Few records in Britain or Ireland to date, but distribution probably coincident with that of P. pungitius. Formerly confused with S. solidus. z zyxwvutsr A KEY TO THE SPECIES OF CESTODES 52 1 zyxwvutsrqponmlk zyxwvutsrq zyxwvu FIG.I . Vuliporu cumpy/uneris/rutu. Anterior part oflarva with rostellum extended to show hooks. Note two circles of large and small hooks, respectively (arrowed). Host: carp, Cyprinus curpio. Scale bar 0.1 mm. FIG.2. Vuliporu cutnpylnncristro/u. Whole larva, incompletely relaxed with rostellum withdrawn. Two suckers visible (arrowed). Scale bar 0.1 mm. FIG.3. Ligulu intestinalis. Anterior part of plerocercoid, showing scolex cone and annulation as broken circles (arrowed). Hosts: Cyprinidae. Scale bar 1 mm. Shoulder of first annulation nearly straight-edged (see three arrows in Fig. 8). Parasite of Gasterosteus aculeatus Schistocephalus solidus (Figs 7,8). Plerocercoid in body cavity of three-spined stickleback, C. aculeafus L. Copepods are first intermediate hosts, piscivorous 522 zyxwvu J . C. C H U B B ET A L . zy zyxwv A KEY TO THE SPECIES OF CESTODES 6. 7. 8. 9. 523 birds or mammals definitive hosts. Widespread throughout British Isles, coincident with G. aculeatus. Often locally abundant, but sporadic in occurrence. Scolex with four three-pronged hooks and two shallow bothria (adhesive depressions) Triaenophorusnodulosus (Fig. 9). Plerocercoid encapsulated by host-response tissue, normally in liver, less commonly other viscera. Principal host for plerocercoid in British Isles is perch, PercaJIuviatilis L. Copepods are first intermediate hosts. Adult worms in intestine lumen of pike, Esox lucius L. Widespread, but only in waters containing E. lucius. Scolex lacking three-pronged hooks 7 Scolex with four, spinous tentacles and two bothridia (also adhesive depressions) Hepaloxylon squali (Fig. lo). Plerocercoid larvae attached to viscera or musculature of salmon, Salmo salar L. Infections acquired and established at sea. Adult worms parasitic in intestine of marine selachians. Larvae reported sporadically in British Isles from S. salar caught during spawning migration into fresh waters. Scolex without armed tentacles 8 Scolex not extended after relaxation of living worm in cold water for about 1 h; hence, the two bothria of the scolex remain concealed by forebody of plerocercoid. Parasitic in somatic musculature, but may be encapsulated in viscera Diphyllobothrium latum (Fig. 11). Plerocercoid very annulated, at least under SEM. Free in somatic musculature of Esox lucius and PercaJIuviatilisbut may be encapsulated in viscera. Copepods are first intermediate hosts. Adult worms endemic in man in Ireland, and formerly frequently reported. Recent records in Britain from immigrants. Scolex becomes extended after relaxation of living worm in cold water for about 1 h, thus the two bothria of scolex are readily visible. Usually encapsulated in viscera ( D . dendriticum, D. ditremum) or in liver ( D . vogeli) 9 Bothria wide open after relaxation of plerocercoid (Fig. 12). Annulation usually clearly apparent immediately behind scolex Diphyllobothrium dendriticum (Fig. 12). Plerocercoids encapsulated in or on viscera. Common, with D. ditremum, in Salmonidae, less frequently Thymallidae, Coregonidae and Gasterosteidae. Frequent in montane lakes. Copepods are first intermediate hosts. Gulls (Laridae) appear to be z zyxwvu FIG.4. Ligulu inresrinulis. Apical view of scolex. Note division into two parts (arrowed). Scale bar I mm. zy FIG.5. Schisfocephulus pungirii. Lateral view of anterior end of plerocercoid. Note complete annulation. Scolex arrowed. Host: ten-spined stickleback, Pungitiuspungifius. Scale bar I mm. FIG.6. Schisfocephulus pungifii. Apical view of scolex. Note shoulder of first annulation curved along its length (three arrows). Scale bar I mm. 524 zyxwvutsrq zyxwv zyxwv J . C . CHUBB ET A L . zy zyxwvut Frc. 7 . Schistocephulicy solidus. Anterior end of plerocercoid. Note complete annulation. Scolex arrowed. Host: three-spined stickleback, Gasterosieus aculeatus. Scale bar I mm. FIG. 8. Schisfocephalus solidus. Apical view of scolex. Note shoulder of first annulation nearly straight- edged (three arrows). Scale bar I mm. natural definitive hosts in British Isles, but piscivorous mammals or man can also act as hosts. Bothria more or less slit-like after relaxation of plerocercoid. (Figs 13, 14, 15). No annulation apparent immediately behind scolex 10 zyxwvutsrq zyxw A KEY TO THE SPECIES OF CESTODES 525 zyxwvutsrqp zy FIG.9. Triaenophorusnodulosus. Anterior end of plerocercoid. Note bothrium (B) and the protruding tips of the three-pronged hooks (arrowed). Host: perch, Percaj7uviatilis; less commonly other fishes. See also Fig. 21. Scale bar 0.5 rnm. FIG.10. Heparoxylon squuli. Anterior end of plerocercoid. Note the four spinous tentacles and bothridium (arrowed). Host: salmon, Salmo salar. Scale bar I mm. 526 J. C. CHUBB ETAL. zyxwv zyxwvutsrqponmlk zyxw zyxwvu FIG.I I . Diphylluborhriumlutum. Anterior end of plerocercoid. Note scolex (arrowed) still retracted within forebody of larva. Hosts: pike, Esuw lucius, perch, Percufluviutilis. Scale bar 1 mm. FIG.12. Diphylluborhrium dendriricum. Anterior end of relaxed plerocercoid. Note wide open bothria and annulation immediately behind scolex (both arrowed). Hosts: Salmonidae, Coregonidae, Thymallidae, Gasterosteidae. Scale bar 0.5 mm. zyx FIG.13. Diphylloborhrium dirremum. Scolex and neck of plerocercoid. Note slit-like bothria widening slightly towards the anterior of the scolex, absence of annulation behind scolex, and distinct neck. Hosts: Salmonidae, Coregonidae, Thymallidae, Gasterosteidae. Scale bar I mm. 10. Scolex opaque-white, contrasting with translucent body of plerocercoid, after relaxation, and when fixed in formaldehyde. A distinct neck usually separates scolex from body of the larva (Fig. 13) Diphyllobothrium ditremum (Fig. 13). Plerocercoids encapsulated in or on viscera. Common, with D. dentriticum, in Salmonidae, less frequently Thymallidae, zyxwvutsr zyxw zyxwvu A K E Y TO THE SPECIES OF CESTODES 527 Coregonidae and Gasterosteidae. Frequent in montane lakes. Cormorants, Phalacrocorax carbo carbo (L.), appear to be natural definitive hosts in Britain and Ireland. Scolex and body of plerocercoid neither of contrasting opacity nor separated by a distinct neck (Fig. 14) Diphyllobothrium vogeli (Figs 14, 15). Plerocercoids usually in liver tissue of Gasterosteus aculeatus. Few records for Britain, none for Ireland, perhaps owing to confusion with other species of Diphyllobothrium. Adult worms in gulls (Laridae). ADULT CESTODES zy zy zy 1 1. Worms with single set of genitalia (monozoic). Body lacking annulation (= segmentation) 12 Worms with serially arranged, multiple sets of genitalia (proglottids). Body (strobila) with external annulation (=segmentation) which may or may not coincide with proglottids 15 12. Scolex blunt, with shallow bothria. Small worms, about 2-3 mm long when mature Arch ige tes sieb oldi (Fig. 16). Normally matures and completes life cycle in tubificid oligochaete, although it has been recorded from roach, Rutilus rutilus (L). See Discussion for other species of Archigetes found as adults in oligochaetes in the British Isles. Scolex blunt or fan-like, without bothria. Gravid worms usually 5 mm or longer 13 13. Scolex blunt, without any obvious external features Caryophyllaeides.fennica (Fig. 17). Parasite of intestine of Cyprinidae, especially Rutilus rutilus. Widespread occurrence where cyprinids are present. Intermediate host Stylaria lacustris (L.) (Oligochaeta). Ovary an inverted A-shape. 14 Scolex fan like, often wider than body 14. Anterior margin of scolex with lobes or indentations more or less in one plane when contracted or relaxed. Long constricted neck present Caryophyllaeus laticeps (Fig. 18). Parasite of bream, Abramis brama (L.), Rutilus rutilus and less frequently other Cyprinidae. Tubificid worms are intermediate hosts. Ovary an H-shape. Widespread. Anterior margin of scolex deeply scalloped in three dimensions. Neck constriction absent Caryophyllaeus fimbriceps (Fig. 19). Recorded from barbel, Barbus barbus (L.), and dace, Leuciscus leuciscus (L,), by Kennedy (1974), who expressed doubt about the identification. We have been unable to obtain material of this species, so figure the original drawing of the scolex from Annenkova-Khlopina (1919). 528 zyxwvutsrq 16 J . C. CHUBB ET AL. 17 -V zyxw zyxwvutsrq zy zyx FIG.14. Diphylloborhrium vogeli. Lateral view of scolex and forebody of plerocercoid. Note slit-like bothria and absence of both annulation and distinct neck behind scolex. Host: three-spined stickleback, Gasrerosteusaculearus. Scale bar I mm. FIG.15. Diphylloborhrium vogeli. Apical view of scolex. Scale bar 1 mm. FIG.16. Archigetes sieboldi. Whole worm in the oligochaete host. Note scolex with bothrium (arrowed). Eggs can be clearly seen in the uterus. Hosts: Limnoddus spp., Cyprinidae. Scale bar 1 mm. FIG. 17. Curyophyllaeides ,fennica. Note blunt scolex (arrowed) without any external features. Hosts: Cyprinidae. Scale bar 1 mm. A zyxwvuts zyxwv zyxw KEY T O THE SPECIES OF CESTODES 529 zyxwvutsrqpo FIG.18. Curw)phy//uru.r/u/iwps. Note rounded lobes and indentations of scolex more or less in one plane. Hosts: Cyprinidnc. Scale bar I mm. zyxwvutsrq FIG.19. f r r r ~ u p / ~ ~ f / u ~ u s , f ~Drawing ~ ~ i c ~ , (enlarged p.s. from Annenkova-Khlopina, 1919)of scolex to show deep scalloping in three dimensions. Hosts: Cyprinidae. Scale bar 1 mm (estimated). FIG.20. C~~tr//roc.ep/iaha /runculus. Funnel-like scolex (arrowed). Hosts: Salmonidae, occasionally other lishes. Scale bar I mm. FIG.21. Triumophorus nodu/osus. Apical view of scolex. Note tips of the three-pronged hooks (arrowed). Scc also Fig. 9. Host: pike, Esox lucius. Scale bar 0.25 mm. 15. Scolex funnel-like Cyathocephalus truncatus (Fig. 20). Parasitic in pyloric caeca of Salmonidae, occasionally grayling, Thymallus thymallus (L.), eel, Anguillu anguilla (L.), Eso.u lucius, stone loach, Noemacheilus barbatula (L.),and Perca ,fluviatilis. Procercoids (caudate adults, Freeman, 1973) in haemocoel of Gammurus pulex (L.). Widespread in streams with populations of G. pulex. Scolex not funnel-like 16 16. Scolex with four three-pronged hooks, their bases embedded in tissue 530 zyxwvuts zyxwvuts zyxwvu J. C. CHUBB E T A L . zyxwvuts FIG.22. Earhyborhriurn recrungulurn. Scolex to show absence of apical disc and open bothria (both arrowed). Host: barbel, Earbus burbur. Scale bar 1 mm. FIG.23. Earhyborhrium recrungulum. Proglottids showing laterally placed vitelline glands (arrowed). Scale bar I mm. FIG.24. Eorhriocephalus acheilognarhi. Scolex: note inverted heart-shape. Hosts: Cyprinidae. Scale bar 1 mm. FIG.25. Eorhriocephalus ucheilognarhi. Scolex: to show apical disc not distinctly separated from scolex (arrowed) and slit-like bothria. Scale bar 1 mm. Triaenophorus nodulosus (Fig. 21). Adult worms specific to intestine of Esox lucius. Copepods as first intermediate hosts, plerocercoids encapsulated in liver of fishes (see 6 above). Widespread, coincident with E. lucius. Scolex without hooks 17 17. Scolex with two bothria 18 Scolex with four suckers 23 18. Scolex lacking apical disc. Vitelline glands located laterally in proglottis Bat hybo thrium rec t angulum (Figs 22,23). Adult worms in intestine of Burbus barbus in R . Ouse system, Yorkshire (Andrews 8i Chubb, 1984). Bothria wide-open when scolex relaxed in cold water. zyxwvutsr zyxwvut zyxw A KEY TO THE SPECIES OF CESTODES 53 1 zyx Scolex with apical disc. Vitelline glands not located laterally in proglottisl9 19. Apical disc not distinctly separated from scolex (Figs 24, 25, 26). Strobila without dorsal and ventral furrow 20 Apical disc distinctly separated from scolex (Figs 27,28,29). Strobila with 21 dorsal and ventral furrow (Figs 28,29) 20. Scolex an inverted heart-shape, apical disc square, bothria slit-like Bothriocephalus acheilognathi (Figs 24, 25). Adult worms parasitic in intestine of cyprinids, occasionally other fishes. Vitelline glands evenly distributed throughout cortical layer of proglottis. Copepods are intermediate hosts. An imported species currently most likely to be found in cultured or ornamental fishes. Scolex longer than wide when relaxed, apical disc bilobed, with two obvious indentations, one above each of the shallow, open bothria Bothr iocephalus claviceps (Fig. 26). Adult worms parasitic in intestine of Anguilla anguilla. Immature individuals occasionally found in other species of fishes. Copepods serve as intermediate hosts. Widespread through Britain and Ireland, but adults specific to A. anguilla. 21. Apical disc of scolex with four indentations Eubothrium crassum (Fig. 27). Adults parasitic in pyloric caeca of Salmo salar, brown trout, S. trutta L., and rainbow trout, S. gairdneri Richardson. Copepod species serve as first intermediate hosts, with plerocercoids or juvenile worms in the intestine of a variety of non-salmonid fishes. Two races of E. crassum are found in the British Isles, one in freshwater S. trutta and the other in anadromous S. salar and S. trutta (Andersen & Kennedy, 1983). Common throughout British Isles. 22 Apical disc of scolex with two indentations (Figs. 28,29) 22. Apical disc with smooth, flat surface Eubothrium salvelini (Fig. 28). Adults parasitic in pyloric caeca of charr, Salvelinus alpinus (L.). Copepods serve as intermediate hosts. Found only in waters with S. alpinus. Apical disc with prominent boss at centre Eubothrium fragilis (Fig. 29). Adults parasitic in intestine of allis shad, Alosa fallax (Lactpide). Our materials from R. Severn. 23. Genus Proteocephalus Four suckers on scolex, often with an apical glandular area which has been erroneously described as a fifth sucker. Copepods are intermediate hosts. Twelve species are known to occur in Britain and Ireland. The adult worms are specific to a single species of fish. P. torulosus is an exception, occurring in a range of Cyprinidae. Table I facilitates the identification of species of Proteocephalus, but should only be used when mature and gravid worms are found in the appropriate species of fish, since juvenile Proteocephalus are transient members of the intestinal fauna of zyxwvu 532 zyxwvuts zyxwvu zyxwvutsr J . C . CHUBB ET A L . zyxwvuts zyx zyxw zyx FIG.26. Eurhriocephuluv cluviceps. Note scolex longer than wide and the bilobed apical disc with an indentation aboveeach bothrium (arrowed). Host: eel, Anguillu unguillu. Scale bar 0.5 mm. FIG.27. Eubothrium c r u s s u ~ Note . four indentations (arrowed) in prominent apical disc of scolex. Hosts: salmon, Sulmu sulur, brown trout. S. rruttu, rainbow trout, S. guirdneri. Scale bar 1 rnm. FIG.28. Euborhrium sulvelini. Note two indentations on prominent apical disc of scolex (arrowed) and strobikd with dorsal and ventral furrow (also arrowed). Host: charr, Sulvelinus alpinus. Scale bar 0.5 mm. FIG.29. Eubothrium frugilis. The prominent central boss and two slight indentations of apical cap are arrowed. Host: allis shad, Alusufulkux. Scale bar 0.5 mm. zyxwvutsr zyxw zy A KEY TO THE SPECIES OF CESTODES 533 zy zyxwvu species of fishes in which they cannot mature. Relevant species of fish are listed, in alphabetical order of generic name, in column 1 of Table I. The appropriate species of Proteocephalus specific to these fishes are given in column 2, with evidence for the host specificity summarized in column 3 . Where we have been able to provide photographs of scolices of the species, the figure number is given in column 4. Notes about occurrence in the British Isles are provided in column 5 . In this paper, we have provided neither full descriptions nor a key to the species of Proteocephalus; we hope to prepare these for a later publication. However, Table I1 gives details of some features of proglottis morphology of species of Proteocephalus recorded in the British Isles. Full descriptions of each of these species can be found in the sources indicated. It must be stressed that mature and gravid individuals of Proteocephalus are necessary for species confirmation using morphological characters, and that, even along the strobila of one worm, quite dramatic variations in arrangement, number and size of the internal organs can occur. At this time we recommend submission of Proteocephalus materials to a specialist for identification. Voucher specimens, with pertinent data, should be deposited in a national museum, so that the identity can be validated at a later date, if necessary. V. DISCUSSION In compiling this checklist and key we have included all of the species of tapeworms known to us from freshwater fishes in Britain and Ireland. It is hoped that if species occur which have not so far been reported, the publication of this key will aid in their discovery. It is also hoped that the key will stimulate interest in, and correct identification of, these interesting and important parasites of fishes. The authors will welcome any comments for improvement of the key, records of the occurrence of the species, and materials for identification. If specimens do not readily conform to the characters we have used, it is vital that they be submitted to a specialist for checking, since it is quite possible that, for a variety of reasons discussed in detail below, the user may encounter species not currently considered part of the fauna of the British Isles. In drawing attention to the following specific instances, we hope to stimulate further research into the occurrence and distribution of cestodes in the British Isles. Four species of Caryophyllidea are given in the checklist; however, within the genus Archigetes three additional species are known to occur in oligochaetes of the family Tubificidae in the British Isles (Kennedy, 1965a,b): A . sieboldi, A . hrachyurus Mrazek, 1908 and A. limnodrili (Yamaguti, 1934). Only A . sieboldi has been recorded from the intestines of British fishes (Shillcock, 1972) although both A . hrachyurus and A . limnodrili have been found in fishes in other parts of the world. Kennedy (19656)provided a key to five species, two of which have not been recorded from Britain. The three species, A . brachyurus, A . iimnodrili and A . sieboldi can be distinguished as follows (modified after Kennedy, 1965b): 1 . In the anterior part of the body testes beginning after the vitellaria and not arranged in longitudinal rows. Testes number 75-95 (mean 90) Archigetes sieboldi In the anterior part of the body testes beginning level with or in front of the 2 vitellaria and arranged in longitudinal rows 534 zyxwvu J. C. C H U B B E T A L . zy FIG.30. Proteocephalus macrocephalus. Note absence of central glandulararea as surface feature. Host: eel, Anguilla anguilla. Scale bar 0.25 mm. FIG.31. Proteocephalusexiguus. Thecentral glandulararea (arrowed)is often incorrectly described as a fifth apical sucker. Host: gwyniad, Coregonus lavarefus. Scale bar 0.25 mm. FIG. 32. Proieocephalus torulosus. An optical microscope photograph. Hosts: Cyprinidae. Scale bar 0.25 mm. FIG.33. ProfeocephalusJilicoIlis. Host: three-spined stickleback, Gasferosteusaculeafus. Scale bar 0.25 mm. 2. Testes arranged in rows, of 30-40 each, 12&159 (mean 137) in total Archigetes brachyurus A K E Y TO T H E SPECIES OF CESTODES 535 z zyxwvutsrq zyxw zyxwvutsr FIG.34. fro/eocephalus ocellurus. Note indistinct glandular area (arrowed) at apex of scolex. Host: perch, zyxwvut PercoJluviurilis. Scale bar 0.25 mm. FIG.35. Proreocephalusneglecrus. Note central glandular area (arrowed). Host: brown trout, Salrno rrurra. Scale bar 0.25 mm. FIG.36. Proreocephalus oscularus. This worm was removed from the host by anthelmintic treatment; hence, note eversion of sucker tissue and central glandular area (arrowed). Host: wels, Silurus glanis. Scale bar 0.25 mm. Testes 39-63 (mean 50) Archigetes limnodrili As the records of Caryophyllaeus jimbriceps in Barbus barbus and Leuciscus leuciscus from Boston, Lincs and the River Avon, Hants were regarded as doubtful by the original author (Kennedy, 1974), we attempted to obtain new materials of this species from overseas for comparative purposes, but failed. Consequently, we zyxwvutsrqpo zyxwvutsr zyxwv zyxw zyxwvutsrqponmlkjihgf zy zyxwvutsrqponmlk zyxwvuts TARLE 1. Identification of species of Proreocephulusrecorded in the British Isles by means of host specificity. See text for explanation Fish host species Proieocephulus species (1) (2) A I I ~ U ~ Iariguillu. ILI cel Corcgonirr ulhulu. P. r~iucroccpiialus P. pollanicola vcndance. pollan Cori,~.~oriu.s lulwetus, P. c*siguus schclly. powan, gwyniad Cyprinidac: Lcuciscus cepholus. chub; L . 1c.uci.rc.ir.v.dace; Riirilus ruriliis, roach P. rorulosus Go.stiwi.sriw.suidiiarus. P..filicollb rufTc Nocni~iclieilushurhutir1ir.t Fig. number (4) All records of mature worms in British Isles from A . anguilla Recorded only from C. albula (Gresson & Corbett, 1954) Recorded only from C . luvaretus (Chubb, 1963) All records in British Isles from cyprinid hosts (Kennedy, 1974) 30 31 32 - P. strgirrus Specific to N.barbalulus in U.S.S.R. - P. ocellarus Demonstrated experimentally (Willemse, 1969) Demonstrated experimentally (Willemse, 1968) 34 P. iwnua 33 stone-loach Piwu.fluiiuri1i.s. perch Pungirius pungiriirs. P. umhiguus ten-spined stickleback Sulmo Kuirilneri, - - P. parallaclicus rainbow trout Sulnio trurra. P. nl~glecrus brown trout Sulwlinus ulpinus. Demonstrated experimentally (Priemier, 1980) 35 - P. species? charr S i l i o i r . ~g1ani.v. wels P. o.sculuru.s Only in S. glanis in Europe and U.S.S.R. Notes about occurrence in British Isles (5) Widespread in British Isles (see Kennedy, 1974). In Ireland (J. C. Chubb, unpubl.) Demonstrated experimentally (Willemse, 1968) Demonstrated experimentally (Willemse, 1969) three-spined sticklcback Gyninoccpiialus ccrnuu, Evidence for host specificity (3) 36 Lough Neagh, R.Bann, Ireland (Gresson & Corbett, 1954). See Discussion Llyn Tegid and Loch Lomond (Chubb, 1963 and unpubl.). See Discussion Widespread in cyprinid populations (see Kennedy, 1974) Widespread in British Isles (see Kennedy, 1974; Conneely & McCarthy, 1984) Not reported in British Isles to date, but gravid Proreocephalusfrom G. cernua should be critically examined. See Discussion In British Isles in Jersey (Kennedy er al., 1986)and Yorkshire (C.Andrews, unpubl.) Recorded in England (see Kennedy, 1974)but not Ireland P.jlicollis recorded in P. pungitius by Dartnall (1973) and Conneely & McCarthy (1984). In light of Willemse (1968) experiments these records need reassessment. See Discussion Single record, Kilrea, Antrim, Ireland (Anne & Ingham, 1972). See Discussion Recorded in Welsh River Dee system (Chubb, 1977; Rahim, 1981) Proreocephalusspecies, as yet undetermined, occur in S. alpinus in Windermere and Loch Ness (J. C. Chubb. unpubl.) Only recorded from a Yorkshire fish farm (Andrews & Chubb, 1984). See Discussion z zyxwvutsrqp zyxwvu zyxw 537 A K E Y TO THE SPECIES OF CESTODES TABLE 11. Some features of proglottis morphology of species of Proteocephalus recorded in the British Isles Ratio cirrus sac No. of lateral length to width pouches on each of proglottis side of uterus Proteocephalus species No' Of testes per proglottis P . ambiguus P . cernua P . exiguus P .jlicollis P . macrocephalus P. neglectus P . ocellatus P . osculatus P . parallacticus P . pollanicola 30 60-80 24(30-40)54 45 80-1 10 63-77 about 50 180(250)424 45-92 60-75 1:4/3:10 1 :4/1:5 1 :2 1 :3/1:4 1:6/1:7 1:3 4:10 2:5/2:9 1:2 1 :4 5-7 5-8 5(8)14 7-8 7-9 5-9 8 5-9 7-12(15) 3-9 3555 60( 100)150 1:3/1:4 1:4/1:8 4-7 3-7 P . sagittus P . torulosus source of data Willemse, 1968 Willemse, 1969 Freze, 1965 Willemse, 1968 Willemse, 1969 Freze, 1965 zyxwv Willemse, 1969 Freze, 1965 MacLulich, 1943 Gresson & Corbett, 1954 Freze, 1965 Freze, 1965 Note: Priemer (1982) figures P. cernua. P. exiguus, P.jilicollis. P. macrocephalus, P. neglectus, P. ocellatus (as P. percae), P. osculatus, P . pollanicola. P. sagitrus and P. torulosus. have reproduced, in enlarged form, the figure of the scolex from the original description (Annenkova-Khlopina, 1919). The scolex of C .fimbriceps appears to be sufficiently distinct from that of C . futiceps to allow differentiation of the two species. Khawiasinensis Hsu, 1935was described from Cyprinus carpio in China but since that time it has spread with cultured cyprinid fishes to many parts of the world. It is probably only a matter of time, therefore, before K. sinensis is found in Britain. The scolex is broad, flat and h b r i a t e , but not separated from the body by a welldefined, constricted neck (Schmidt, 1986). Superficially, however, specimens of K. sinensis which we have examined from Algeria could easily be mistaken for a species of Caryophyffueus.K. sinensis belongs to the family Lytocestidae, members of which have the vitellaria entirely cortical, with the testes medullary. By contrast, worms of the family Caryophyllaeidae, to which C. faticeps and C . jmbriceps belong, have both the vitellaria and testes entirely medullary. Accordingly, transverse sections are necessary to separate K . sinensis from C . futicepsor C.fimbriceps. Even with such sections, great care must be taken in searching for the parenchymal musculature of K. sinensis which separates the vitelline glands from the testes, as the bundles of muscle are discontinuous and not strongly manifest. Of the order Trypanorhyncha, only plerocercoids of Hepatoxyfon squafi have been found in fresh waters, in Safmosafur returning from the sea to spawn. Careful searching of other anadromous fishes could reveal more species of trypanorhynch larvae. As the structure of the scolex and, especially, the arrangement ofhooksand spines are highly specific, other species should be readily distinguished from H. squafi. A number of remarks are necessary concerning members of the order Pseudophyllidea. Two species of the genus Digramma could occur in the British Isles, but zyxwvu 538 zyxwvuts zyxwvu J . C. CHUBB E T A L . so far have not been reported. Members of this genus closely resemble species of Ligula but, whereas a single series of genital complexes occurs along the length of the strobila of Ligula, there are two regular longitudinal rows in Digramma species. Externally, Ligula species have one longitudinal ventral groove, whereas Digramma species have two parallel, longitudinal and ventral grooves. Plerocercoid larvae of Digramma interrupta (Rudolphi, 1810) are primarily parasites of crucian carp, Carassius carassius (L.), Prussian carp, Carassius auratus gibelio (Bloch) and Abramis brama in the U.S.S.R. (Dubinina, 1966) although they also occur less frequently in other species of wild and cultivated cyprinids. D. interrupta plerocercoids in cyprinids. and adults in piscivorous birds, have been recorded in western Europe (Dubinina, 1966), so they are likely to occur in the British Isles. D . nemachili Dubinina, 1957, with plerocercoids in fishes of the genus Noemacheilus, could also potentially occur in British N . barbatulus. There are four species of the genus Diphyllobothrium present in the British Isles. Adult D. latum were formerly reported regularly from man in parts of Ireland, and less frequently (perhaps only) in continental immigrants in Britain (van Bonsdorff, 1977). While this species was probably endemic throughout the British Isles at one time, and until recently in Ireland, there are no modern records of plerocercoids in freshwater fishes. D. dendriticum and D. ditremum plerocercoids are commonly recorded in salmonoid fishes in Ireland, Scotland and Wales, with fewer occurrences in England. D. vogeli is a more enigmatic species: originally described by Kuhlow (1953), the adult worms were obtained from experimental infections of the black-headed gull, Larus ridibundus L.; the plerocercoids were collected from Gaslerosteus aculeatus. In the R. Elbe, Germany they infected 15% of G. aculeatus and were located in the outer layer of the liver, and when placed in physiological saline the larvae were very motile, more so than those of the other species Kuhlow found in Germany. In addition, the long microtriches, 18-35pm, were considered highly characteristic. Chubb (1968), however, regarded adult D. vogeli from L. ridibundus as described by Kuhlow (1953) to be primary strobila of D. ditremum, and Halvorsen (1970) also, as a working hypothesis, regarded D . vogeli as a synonym of D. ditremum. Bylund (1975a,b) subsequently found pronounced differences in the strobila of adult worms of D. ditremum and D. vogelireared in the same species of definitive hosts. Furthermore, differences were also found during an examination of the embryonic hooks (Bylund, 1975c) and gel electrophoresis performed on the whole-body proteins of the adult worms (Bylund, 1977). There seems, therefore, no reason to doubt the distinctness of the two species, D. ditremum and D. vogeli, although it is unusual that the fish host, G. aculeatus, can harbour three species of Diphyllobothrium, D. dendriticum, D. ditremum and D. vogeli, and that two of these species, D. dendriticum and D. vogeli, also utilize Laridae (gulls) as definitive hosts. Further studies of D. vogeli in the field may demonstrate clearer niche-separation between this and the other species, and help to clarify their taxonomic status. In Britain, plerocercoids of D . vogeli have been found at Llyn Padarn, Wales and Loch Ness, Scotland in the livers of G. aculeatus (J. C . Chubb, unpubl.). Larvae of two species of Schistocephalus, S. pungitii and S. solidus, are included in the key. Until recently (Hyslop & Chubb, 1983) S. pungitii was not separated from S. solidus in the British Isles, despite experimental evidence showing that S . solidus procercoids established themselves normally in Gasterosteus aculeatus, zyxwv zyxwvutsr zyxw zyxwvuts A KEY TO THE SPECIES OF CESTODES 539 whereas in Pungitiuspungitius their growth ceased after 6 to 8 days and the larvae were dead by day 11 at 19.5" C and day 14 at 10" C (Orr et al., 1969). Briten (1966) also demonstrated that plerocercoids of S . solidus from G . aculeatus implanted by surgical transfer into P. pungirius failed to grow and showed degeneration of microtriches after 6 days, but survived for long periods. Thus, the records of S . solidus from P . pungitius (Kane, 1966; Dartnall, 1973) must be referred to S . pungitii. We have not included ' Scolexpleuronectis ' Miiller, 1788 (order Tetraphyllidea) in the key. These larvae, of an unknown number of species of tetraphyllids, are of marine origin and are common in a variety of marine and estuarine fishes. We have seen them in flounder, Platichthysjesus (L.), from the River Dee, Wales which have migrated from the sea into the river to feed. ' S. pleuronectis ' larvae are of small size, usually a few millimetres in length, and of diverse form. Yamaguti (1934) divided them into five types. However, until enough specimens with fully developed scolices are available from freshwater or estuarine fishes for comparison with adult tetraphyllids from marine fishes, it is unlikely that precise identification will be possible. A large number of species of the genus Proteocephalus (order Proteocephala) occur in fishes in the British Isles. Five of these, P.JilicoNis, P . macrocephalus, P . neglectus, P . ocellatus (formerly, but incorrectly, known as P . percae, see Willemse, 1969) and P . torulosus require no further comment. Our record of P . oscufatus is from wels, Silurus gfanis (L.), on a fish farm (Andrews & Chubb, 1984), so it is possible that the cestode may not occur in this fish in the few waters in which it is resident in southern England. Kennedy et al. (1986) reported P. sagittus in Noemacheilus barbatulus from Jersey and suggested that the cestode had colonized the island from France. We have, however, seen P . sagittus in N . barbatulus from Yorkshire ( C . Andrews, unpubl. comm.). The remaining species of Proteocephalus require further study before their precise status in the British Isles is clear. Proteocephalus pollanicola was described from pollan, Coregonus albula (L.), in Lough Neagh, Ireland by Gresson (1952) and Gresson & Corbett (1954). It has not been reported subsequently from anywhere else. However, P . exiguus has been noted from gwyniad, Coregonus fuvuretus (L.), in Llyn Tegid, Wales, and a species, probably also P . exiguus, has been found in C. lavaretus in Loch Lomond, Scotland (J. C . Chubb, unpubl.). As P . exiguus occurs in both C. albula and C. favaretus in the U.S.S.R. (Ieshko & Anikieva, 1980) a detailed reappraisal of proteocephalids from the species of Coregonus in the British Isles is obviously necessary. We are dubious whether Proteocephalus cernua is present in the British Isles. Willemse (1969) was convinced that P . cernua from ruffe, Gymnocephalus cernuu (L.), in the Netherlands was a distinct species. He reached this conclusion on the basis of field observations of host specificity,experimental laboratory infections of fishes and a morphological study of the adult worms. However, his experimental study in this instance did not give decisive results. Wootten (1973) reported a low prevalence (3.6%) and mean intensity (2.0) of P . oceflatus (as P . percae) from G . cernua in Hanningfield Reservoir, Essex. In Percafluviutilis, prevalence (53.6%) and mean intensity (1 3.4) of P . oceflatus were high. Wootten (1973) noted specifically that P. oceflatusin the atypical host G. cernua were infrequent and not mature, so it is likely that he was correct in his identification. In samples of G. cernua from zyxwvu 540 zyxwvuts zyxwvuts zyxwvu zy J . C. CHUBB E T A L . the Serpentine, London (Lee, 1977) and from Llyn Tegid (Bala Lake), Wales ( S . Wild, unpubl. comm.) P . cernua has not been found. However, there is a possibility that some habitats in England where G . cernua is local but abundant will contain P. cernua. Proteocephalusjilicollis has been reported by Dartnall (1973) and Conneely & McCarthy (1984) from Pungitius pungitius. However, according to Willemse (1 968), although the morphological characteristics separating P . jilicollis from Gasterosteus aculeatus and P . ambiguus from Pungitius pungitius were small, experimental infections demonstrated that a high degree of host specificity existed in cestodes from the two hosts. He took eggs from worms in P. pungitius and infected Cyclops strenuus with them. C. strenuus containing larvae were fed to fishes 4-7 weeks after ingestion of eggs. Infections always established in P . pungitius but never in G. aculeatus, nor in other fish species. Willemse (1968) also found it impossible to take adult cestodes from one of the stickleback species and to transfer them experimentally to the other host species, whereas control transfers between fishes of the same stickleback species were always successful. We must assume, as a result of these experiments, that both P . jilicollis and P . ambiguus occur in the British Isles in their respective hosts, G. aculeatus and P . pungitius. It would be appropriate to extend the study of Willemse (1968) by attempting to infect P . pungitius with experimentally reared larvae of P. jilicollis from G . aculeatus. Arme & Ingham (1972) found a species of Proteocephalus in Sulmo gairdneri in Ireland which they considered to resemble P . parallacticus, a north American species from lake trout, Salvelinus namaycush (Walbaum), speckled trout, Salvelinus fontinalis (Mitchill), and Salmo trutta. We suggest that the Irish materials may have been either P. neglectus, found in Salmo trutta in some other parts of the British Isles, or P . exiguus, reported by Priemer & Goltz (1986) from S. gairdneri in the German Democratic Republic. Some other species of Proteocephalus are likely to be identified from freshwater or migratory fishes in the British Isles. For instance, we have recovered juvenile Proteocephalus from Salvelinus alpinus in Windermere, England and in Loch Ness, Scotland. In addition, when migratory fishes such as the smelt, Osmerus eperlanus (L.), are carefully examined, we predict the discovery of P . longicollis (Zeder, 1800) and P. tetrastomus (Rudolphi, 1810). Willemse (1969) found both these species in 0. eperlanus in fresh waters in the Netherlands. Osmerus eperlanus is fairly widespread and common in estuaries and lower reaches of rivers in eastern England (Maitland, 1972). The importation of commercial and ornamental fishes into the British Isles has led to the introduction of several species of cestodes into our fresh waters. Bothriocephalus acheilognathi is one well-documented example (Stott, 1977; Andrewsetal., 1981;Chubb, 1981;Pooletal., 1984; Pool&Chubb, 1985). It isnot yet clear whether this cestode will become established in native fish populations as it has in other European countries. We predicted earlier in this discussion that the caryophyllidean cestode Khawia sinensis will eventually be found in imported Cyprinidae. Throughout the key we have indicated the sites of occurrence of the cestodes within the fishes. In some instances cestodes can locate in alternative organs, but post-mortem effects or careless dissection can also lead to worms being displaced. zyxwvutsr zyxwvutsr zyxwvuts A K E Y TO THE SPECIES OF CESTODES 54 1 A further complication is that the intestines of piscivorous fishes, birds or mammals can temporarily house worms from recently consumed, infected fishes. Thus Esox lucius in Llyn Tegid may often have adult worms of Proteocephafus exiguus in their stomachs, which originated from the pyloric caeca of Coregonus / m a r e f u s . These proteocephalids do not re-establish in the intestine of E. fucius and will either be digested or defaecated. A corollary from the points made in the latter paragraphs of this discussion is that any cestodes which do not conform to the information provided in this key should be submitted to a specialist for identification. We wish to thank Professor A. J. Cain (Department of Zoology, University of Liverpool) and Dr A. F. Brown (Department of Applied Biology, University of Wales Institute of Science and Technology) for reading the manuscript critically. We are also indebted to the following colleagues and friends for providing specimens of cestodes or unpublished data: Dr C. Andrews (The Zoological Society of London), Dr M. Aprahamian (Welsh Water Authority), Professor 0.N. Bauer (Institute of Zoology, Academy of Sciences, Leningrad), Dr A. F. Brown (Department of Applied Biology, University of Wales Institute of Science and Technology), Dr G. Bylund (Institute of Parasitology, Abo Akademi), Dr L. H. Chappell (Department of Zoology, University of Aberdeen), M r A. F. Dearsley (Thames Water Authority), Dr A-R. A-M. Rasheed (Department of Biology, University of Salahaddin, Iraq), M r A. Richmond (Jerveaux Angling Club) and Mr S. Wild. Finally, we thank M r B. Lewis for printing the figures and Mrs L. Christiansen for word-processing the manuscript. zyxwvuts zy zyxw zy zyx References Andersen, K. I. & Kennedy, C. R. (1983). Systematics of the genus Eubothrium Nybelin (Cestoda, Pseudophyllidea), with partial re-description of the species. 2001. Scriptu 12,95-105. Andrews, C. & Chubb, J. C. (1984). Helminth parasites from Yorkshire fishes. Bull. Eur. ASS. Fish Pathol. 4,22-23. Andrews, C. & Chubb, J. C., Coles, T. & Dearsley, A. (I98 I). The occurrence of Bothriocephulus acheilognuthi Yamaguti, 1934 ( B .gowkongensis) (Cestoda: Pseudophyllidea) in the British Isles. J. Fish Dis. 4,89-93. Annenkova-Khlopina, N. P. (1919). (Two new kinds of parasitic worms of the genus Curyophyllueus, found in the intestineofcarp fishes.) Izvest. Ross. Akad. Nauk. Ser. 6 13,97-110. (In Russian). Arme, C. & Ingham, L. (1972). Proteocephalus sp. in rainbow trout, Sulmogairdneri: a new host record for the Palaearctic. Ir. Nut. J . 17,241-242. von Bonsdorff, B. (1977). Diphllobothriasis in Man. London: Academic Press. pp. i-xii, 1-189. BrGten, T. ( 1966). Host specificity in Schistocephulus solidus. Purastiology 56,657-664. Bykhovskaya-Pavlovskaya, I. E., Gussev, A. V., Dubinina, M. N., Izyumova, N. A., Smirnova, T. S., Sokolovskaya, I. L., Shtein, G. A., Shul’man, S. S. & Epshtein, V. M. (1962). Key to the Parasites of Freshwater Fishes of the U.S.S.R.. Moscow & Leningrad: Izdatel’stvo Akademii Nauk SSSR. 776 pp. (In Russian.) Translation Israel Program for Scientific Translations 1964 Cat. No. 1136. Bylund, G. (19754. Delimitation and characterization of Euro an Diphyllobothrium species. Academic Dissertation. Department of Biology, f r bo Akademi, Finland (ISBN 951-648-172-8)23 pp. Bylund, G. (19756). Studies on the taxonomic status and biology of Diphyllobothrium vogeli Kuhlow, 1953. Commentationes Biol. 79, 1-22. Bylund, G. (19754. The taxonomic significance of embryonic hooks in four European Diphyllobothrium species (Cestoda, Diphyllobothriidae). Acta zool. fenn. 142,1-22. Bylund, G . (1977). Protein profiles as an aid to taxonomy in the genus Diphyllobothrium. Z . Parasitenk. 51,241-247. 542 zyxwvutsr zyxwvu zyxwv zyxwvuts J . C. CHUBB E T A L . Chubb, J. C. (1963). On the characterization of the parasite fauna of the fish of Llyn Tegid. Proc. 2001. SOC.London. 141,609-621. Chubb, J. C. (1968). Tapeworms of the genus Diphyllobothrium in the British Isles. Parasitology 58,22P (Abstract). Chubb, J. C. (1977). A review of the parasite fauna of the fishes of the River Dee system. A report for the Central Water Planning Unit, Reading, England. Pp. i-x, 1-107. Chubb, J. C. (1981). 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