Solving parasite-related problems in cultured freshwater fish

SOLVING PARASITE-RELATED PROBLEMS FRESHWATER FISH

IN CULTURED

KALMANMOLNAR Veterinary Medical Research Institute, Hungarian Academy of Sciences 1581 Budapest, P.O.B. 18., Hungary

INTRODUCTION The extraordinary increase of the saltwater fish catch that had taken place in the nineteen-sixties came to a standstill by the middle of the nineteen-seventies. At the same time, the demand for fish as a valuable protein source increased. These factors enhanced the significance of freshwater fish production. Countries with a conventional fish-breeding structure tried to meet the higher demand for freshwater fish by increasing their output, and produced fish by using more and more intensive methods. In the same period, in numerous countries with no fish-breeding history, the building of fish ponds, importation of fish species of proven breeding value, and selection of indigenous fish species for breeding purposes were started. The extent of these activities varied, depending on the existing conditions and requirements. Parallel with the development of fish breeding, new problems of fish health have emerged. In countries having a highly developed fish breeding, the more frequent incidence of fish diseases (including parasitoses) was attributable, first of all, to intensive management and polyculture rearing. Fishes reared in such systems at high densities were affected also by parasites whose pathogenicity had not been known previously. In countries having no fish-breeding traditions (mainly in Asian, African, and South American countries), mostly the introduced pathogens gave rise to health problems under the climatic conditions favouring them and, less frequently specific parasites of indigenous fishes acquired economic significance. To prevent the economic losses inflicted by fish diseases, a whole series of fish health institutions has been established in European countries, North America, Japan, and China. In these institutions, fishparasitological examination and research have played a very important role. The study of fish parasites commenced in the majority of developing countries as well; however, in the latter countries research has got only as far as surveying the parasite fauna. No reliable data are available on the economic losses caused by fish parasites. The surveys conducted so far indicate that among salmonids the viral and bacterial diseases, while in carp farms the parasitoses have a greater significance. The losses inflicted by parasites are hard to assess. In the majority of cases it cannot be decided whether the losses are due directly to the parasites, to parasitoses accompanied by bacterial and viral diseases, or inadequate feeding and management, inappropriate treatments or other stressors can be considered the sole aetiological factors. Specialists assessing the damages are inclined to attribute greater significance to parasites easily visible with the unaided eye (Bothriocephalus, Piscicola, Lernaea) than to protozoa which are demonstrable only microscopically. Recently, the parasitic infections of fishes of economic importance have been reviewed by Bauer, Egusa & Hoffman (1981) while the therapeutic compounds available for their control by Hoffman (1983) and Moore, Mitchell, Griffin & Hoffman (1984). Surveys of this type are rendered more difficult by the large number (by now several dozens) of fish species reared in different climatic zones, by different methods and for various purposes; therefore, it is almost impossible to discuss the emerging problems by a uniform approach. The problems emerging in salmonid cultures which are usually isolated from natural waters and operate with clean, cold water are different from those occurring in fish ponds of the temperate zone or the tropics. Parasites have a different role in sparsely populated ponds with large surfaces and in intensive cage or enclosure rearing.

319

320

K. Molndr PARASITOSES

IN FISH CULTURES

Purasitoses in salmonid cultures

The study of parasitic diseases of cultured trout and salmonids has long-standing traditions. Most of the parasitoses have been known for nearly a hundred years. Of the causative agents of these diseases the sporadically occurring helminthiases e.g. diplostomosis, crepidostomosis, eubothriosis, have lesser importance in cultured salmonid stocks. In everyday pond farm practice protozoan parasites of wide host range like the flagellate Ichthyobodo, Hexamita, or the ciliated Ichthyophthirius, Chilodonella, Trichodina and Trichophrya species constitute most of the problems. The different myxosporeans are none the less important, mainly because their biology is poorly known and, consequently, they are difficult to control. In recent years such new scientific results have been obtained on the development of myxosporeans which give hope that the diseases caused by these parasites will be overcome successfully. Of the diseases caused by myxosporeans, whirling disease is the best known worldwide. In trout cultures of Europe, whirling disease caused by Myxosoma cerebralis had long been a factor decisively influencing both breeding and the development of rearing systems. The introduction of the causative agent into North America and New Zealand (Hoffman, Dunbar & Bradford, 1962; Waugh, 1975) further increased the significance of this parasitosis, the more so because even at present we do not have an efficacious drug to control it; thus, fish breeders are compelled to take costly preventive measures. The control of whirling disease is hampered by the scarcity of our knowledge of the mode of infection by Myxosoma. Attempts at infecting fish with Myxosoma spores directly have failed so far. At the same time, trout fry contracted severe infection in spore-containing water. As regards the biology of the parasite, the first significant breakthroughs were the results of Uspenskaya (1957), then Hoffman & Putz (1969) who, as an explanation for the failure of infection experiments performed with spores, suggested that the spores have to undergo a certain aging period to reach infectivity. As regards the development of myxosporeans, Markiw & Wolf (1983) put forth a theory fundamentally changing the previously held views: as a result of their experiments with M. cerebralis, they arrived at the conclusion that the development of Myxosoma requires tubificid intermediate hosts. In their opinion the Myxosporea stages developing in Tubifex are identical with parasites so far known as actinosporeans. If the otherwise convincing experiments of the above-cited authors are confirmed by other researchers, or similar results are obtained on other species of Myxosporea, an entirely new era will begin in the control of myxosporean parasites. Successful experimental reproduction of the infection will permit us to use a more exact method instead of the examinations based on observations. Our knowledge of Myxosporea has broadened with new facts on a third very important disease-proliferative kidney disease (PKD) of rainbow trout fry. Since its first description (Roberts & Shepherd, 1974) several pathogens have been incriminated in the aetiology of this disease. Ferguson & McAdair (1977) found cells resembling parasites whilst Ghittino, Andruetto & Vigliani (1977) found amoebae in the kidney of diseased fish. Later Seagrave, Bucke & Alderman (1980) held responsible organisms similar to Marteilia as causative agents. Finally, Kent & Hedrick (1984) reported the occurrence of the disease and of the unclassified pathogen in trout as well as in Pacific salmon. They regarded the pathogen as a developmental stage of Myxosporea which, in a more advanced stage of development, produces in the renal tubules spores similar to Sphaerospora. Parasitoses in carp farms

Of the diseases occurring in conventional carp farms, parasitoses are considered to be the most important. Here also most of the problems are caused by those common protozoan ectoparasites which are a great trouble also in trout cultures. These parasites affect not only the common carp, a species of fundamental importance in fish production, but also the herbivorous fishes, sheatfish and tenth reared more and more frequently in polycultures as accessory fishes. Of these parasites, undoubtedly Ichthyophthirius multifiliis is the most pathogenic. The disease caused by it, White Spot or Ich, is still controlled by bathing the fish in malachite green solution, a technology which has not changed for 25 years. In Europe and North America the number of parasitoses increased especially at the time when rearing of the Eastern Asian herbivorous fishes and Amur wild carp was started in these continents. Some of the parasites introduced with the above fishes, e.g. monogeneans, caused disease among the introduced fishes, while other, e.g. Bothriocephalus acheilognathi and Khawia sinensis produced infection and disease among the indigenous fish species. Myxosporeans of carp cause considerably less damage but set more tasks for research. A large body of new knowledge of these parasites has been obtained in recent years. Research results have revealed that numerous new varieties may exist as regards the mode of development of Myxosporea within the fish, a process that was considered complicated already before. The first remarkable result was that of Csaba

Freshwater fish parasites

321

(1976) who described in common carp blood an extracellularly proliferating protozoan parasite whose taxonomic place was unknown at that time. This was followed by the reports of Kovacs-Gayer, Csaba, BCkCsi, Bucsek, Szakolczai & Molnar (1982) and Korting (1982) according to which swimbladder inflammation (SBI) of the common carp was caused by a protozoan that seemed to be a developmental stage of Myxosporea. Subsequently, as a result of their light- and electron-microscopic studies, Csaba, Kovacs-Gayer, BCkCsi, Bucsek, Szakolczai & Molnar (1984) arrived at the conclusion that the protozoan developmental stages occurring in the blood and swimbladder and developing by internal cleavage corresponded to developmental stages of Sphuerosporu renicolu. The above-listed results open a new chapter in the research of Myxosporea and demonstrate that, as those of the causative agent of the proliferative kidney disease of trouts, the various developmental stages of also other Sphaerosporu-like myxosporidians may develop in different organs, and that the excretion of spores, which is a stage indifferent from the host’s aspect, might be preceded by a stage which is of great importance in pathogenesis (swimbladder inflammation, proliferative changes in the kidney). Dactylogyroses which were so significant in the first decades of the century have lost much of their economic importance because adequate control is available. In carp farms tapeworms are none the less important. Khawia sinensis, a specific parasite of the common carp, has become widespread in Asia as well as in Europe, and Bothriocephulus acheilognuthi, a species able to infect all cyprinids, occurs practically all over the world. The economic losses inflicted in pond farms by these undoubtedly pathogenic parasites may be reduced by using drugs of adequate efficacy. On a world scale, one of the most important parasitoses of carp farms is Lernuea infection. Let-mm cyprinacea is a long-known parasite in Europe; however, it has been causing severe economic losses since the introduction of herbivorous fish species into Europe. Poddubnaya (1978) is of the opinion that the outbreaks of lernaeosis are connected with the importation of L. eleguns, a species similar to L. cyprinuceu but having a greater ability to spread. Parasitoses in catfish cultures

The parasitic diseases of the channel catfish, a species cultured under conditions resembling those of carp farms but in smaller and more densely populated ponds, create similar problems and tasks as those of cyprinids. The main task is to control protozoan ectoparasites. Myxosporidians play an important role also in channel catfish cultures. According to Minchew (1977) and McCraren, Landolt, Hoffman & Meyer (1975), of the myxosporidians Henneguyu spp. may give rise to massive infection. Henneguyu exifis, a species infecting the gills, produces either intralamellar or interlamellar infection, of which the latter is accompanied by considerable mortality (Current & Janovy, 1978). Lernueu infection may be as significant in channel catfish cultures as in carp farms (Hoffman, 1976). Parasitoses in eel cultures

Parasitic diseases of the eel are characterized by specific problems. Like carp farms and catfish cultures, eels are cultured at a higher temperature, but are kept in concrete basins with ample water flow-through at a density similar to that applied in trout cultures. In this system, rearing of fish free from ectoparasitic protozoans and monogeneans can be achieved only if regular preventive antiparasitic bathings are incorporated in the technology. The parasite fauna and parasitoses of Pacific eels have been reviewed by Hine (1978) and Boustead (1982), the parasite of the American eel by Crane & Eversole (1980), while regarding the antiparasitic drugs applicable against eel parsites ample data were furnished by Hinton & Eversole (1979). Of the helminthiases, Pseudoductylogyrus infection described by Ogawa & Egusa (1976) is the most significant. According to Imada & Muroga (1978, 1979), this parasitosis may cause considerable losses by deaths; however, like other monogenean infections, it can be controlled by organophosphate treatment. During experimental fish introductions, Pseudoductylogyrus unguiflue and P. bini have entered Europe and at present, together with Gyroductylus unguillue, they are common parasites of the European eel (Molnar, 1983; Lambert, le Brun & Pariselle, 1984). One of the most significant eel parasitoses, i.e. Myxidium infection of various eel species, is also caused by myxosporidians. Intensive infection of American eels was reported by Ghittino, Smith & Glenn (1974), that of the Pacific eels by Hine (1980), while of the European eel by Copland (1983). The significance of myxidiosis is even greater because of the fact that, for lack of efficacious drugs, in eel cultures high hygienic standards, similar to those characteristic of trout cultures, must be required as a preventive measure.

K. Molnar

322 Parasitoses in tilapia cultures

In tropical and subtropical countries tilapia culture occupies an importasnt position in freshwater fish culture. Only few reports are available on parasitoses occurring in tilapia cultures. Papers on parasites affecting the various tilapia species (Paperna & Thurston, 1969; Paperna & van As, 1983; Sarig, 1971; Landsberg, 1985; Landsberg & Paperna, 1985) suggest that together with the intensification of culturing methods similar problems will emerge in tilapia cultures as those encountered in carp farms. Parasitoses in other cultured

freshwater

fish

There are parasitoses known to affect tropical fish species and minnows cultured as bait fish. The parasite fauna of these fishes has not been clarified yet and it is not clear how pathogenic they may become under culture conditions. The damage done to these fishes by some cosmopolitan species, e.g. Lernaea elegans, is also obscure. Research keeps becoming more and more intensive in this field; the studies of Shotter (1980), the reviews of Khalil (1971) and Paperna (1982) concerning the parasites of African fishes, and the work of Kritsky & Thatcher (1984) on South American fish parasties are worth mentioning. If we consider that all newly described parasites should be regarded as species which, under certain conditions. might become pathogenic, it is clear that the above-listed, and similar, works are of outstanding importance. PRESENT STATUS AND POSSIBILITIES

OF PARASITE CONTROL

In the field of veterinary parasitology, papers on new anti-parasitic drugs appear almost day by day. A broad scale of drugs is available for the control of chicken coccidioses, and numerous good therapeutic comounds are at hand also against diseases caused bv trematodes, tapeworms and nematodes. On the other hand, only a few suitable drugs are available against fish parasites. Very often methods elaborated in the beginning of the century are still being used to control the parasitoses, and the majority of therapeutic compounds is still constituted by chemicals and pesticides; only a few really modern drugs are available, The control of ectoparasites is still based upon bathing the fish in solutions of sodium chloride, formalin, ammonium hydroxide, or potassium permanganate. The first really efficacious antiprotozoan preparation, applicable also under large-scale conditions, was reported by Amlacher (1961) who suggested the use of malachite green for the control of ichthyophthiriosis. Since at that time this chemical has been widely used against various ectoparasitic ciliated and flagellates as well as fungal infections. The other significant discovery of the last 25 years was made by Bailosoff (1963) who reported the high efficacy of the organo-phosphate Neguvon (trichlorfon) against numerous fish parasites. Based on his paper different organophosphate ester preparations (Dipterex, Dylox, Bromex, etc.) were tested by different authors (Saring, Lahav & Shilo, 1965; Grabda & Grabda, 1966; Prost & Studnicka, 1966) for efficacy against monogeneans, leeches and parasitic copepods, and were found to be highly efficacious even when applied in high dilutions in fish ponds. Control of the above parasites is still based upon the use of these compounds. While the ectoparasites of fish are controlled mostly by using simple chemicals and pesticides the anticoccidials used against fish coccidia belong to the “real” drugs. It seems that the coccidiostats that have proved suitable in mammals and birds show good efficacy against fish coccidia as well. Musselius, Ivanova & Laptev (1965) reported the high efficacy of Furazolidone, whereas Kocylowski, Zelazny, Antichowicz & Panczyk (1976) that of amprolium and Nitrofural. Interestingly, so far these preparations have not come into practical use, obviously due to the relatively minor importance of fish coccidioses. Very remarkable results have been obtained by Kano & Fukui (1982) who successfully treated experimentally induced microsporidiosis of eels with Fumagillin. Control of the tapeworms of fish has become necessary simultaneously with the wide distribution of Bothriocephalus acheilognathi. Today niclosamide-containing preparations (Yomesan, Devermin, Phenasal) are used against this parasitosis all over the world (Muzikovskij, 1968; Molt&, 1970; Nakaima, Kitano & Egusa, 1977), the more so because this compound acts also on Khawia sinensis (Sapozhnikov, Muzikovskij & Nazarova, 1971). In the United States, di-n-butyl-tinoxide is used with good results (Hoffman, 1980). This compound has proved to be of good efficacy against Proteocephalus infection of the catfish. According to Molnar (1977) as well as Pool, Ryder & Andrews (1984) praziquantel (Droncit) is as highly effective and safely applicable preparation against bothriocephalosis; furthermore, when applied over prolonged periods, this preparation destroys also Diplostomum metacercariae causing opacity of the eye lens (Bylund & Bjorklund, 1985). Mebendazole has proved to be the drug of choice against larvae of Proteocephaks ambloplitis, a tapeworm parasitizing the largemouth bass (Boonyaratpalin & Rogers, 1984).

Freshwater fish parasites

Of the nematodes Philometroides

parasitizing

the commercially

323

important fishes, so far only the common carp parasite

cyprini (syn. Ph. lusiana) and the eel parasites Anguillicolla crassa and A. globiceps have

been shown to possess economic importance which necessitates their systematic control. Avdosev & Avdoseva (1978) recommended the use of Tiazon against intestinal larvae of Ph. cyprini, while Vasilkov, Tiltin & Suslov (1974) suggested oral or intra-abdominal administration of ditrazine citrate against tissue-parasitic or intra-abdominal stages of the same worm. In the opinion of the latter authors, the success rate of medication can be increased by destroying with organophosphates the cyclops present in the fish ponds which act as intermediate hosts. In the near future, probably similar therapeutic and preventive measures will be necessary to prevent the damage done by Anguillicolla spp. introduced into the European eel cultures. Control of lernaeosis is still based upon the studies of Kasahara (1962) and Lahav, Sarig & Shilo (1964) according to which lernaea-copepods can be killed easily by bathing in organophosphate solutions. According to Yin, Ling, Hsu, Chen, Kuang & Chu (1963) as well as Sarig (1971), the mature copepods can be destroyed by bathing in potassium permanganate solution; however, because of unfavourable experiences due to the high toxicity of the drug, this method has not come into general use. A new drug of reliable efficacy is needed desperately. Dozens of researchers are working on elaboration of such drugs. The number of unsuccessful attempts is obviously high, since Hoffman & Meyer (1974) reported on several dozens of authors who had conducted tests with drugs. FUTURE TRENDS IN PARASITE CONTROL In the future, the scale of antiparasitic compounds will probably broaden in the field of fish breeding. It cannot be excluded that some of these drugs will even be fed regularly, in the form of premixes, in intensive fish culture. However, one thing is certain: improvement of the hygienic standards will remain the most important factor in disease prevention. Today there still exist enormous differences between the hygienic standards of the various branches of fish breeding. Part of the trout and salmon hatching and rearing farms use spring- or well-water in which the fry grow practically free from parasites. These fry will come into contact with parasites only at a later stage of their life. To ensure successful parasite control, in the future the farms lacking such favourable forms of water supply will have to do their utmost to free the inflow water from parasites, using filters, sedimentators, or the ultraviolet light proposed by Hoffman (1974). However, such costly procedures are justifiable only in intensive culture systems, in basins or recirculation cultures (Gratzek, Gilbert, Lohr, Shots & Brown, 1983). Under the conditions of intensive rearing in ponds or cages, a parasite-free (or parasite-deficient) status can be achieved only through regular control included in the technology. This control is based on the chemicals of already proven value, i.e. malachite green and organophosphate esters. According to Strelkov, Solomatova & Kudentsova (1981), cage rearing of cyprinids and trouts especially involves the risk of contracting infection by various parasites. Furthermore, in the opinion of Bauer & Solomatova (1984), under such conditions parasites of such complicated developmental cycle as e.g. Triaenophorus nodulosus may become pathogenic. To replace the chemicals harmful for the fishes and causing water pollution, biological methods seem to methods of control, e.g. that elaborated by Wolf & be the most appropriate. Of these, “vaccination-like” Markiw (1982) against ichthyophthiriosis, are especially interesting. The latter authors dipped rainbow trouts in a solution of Tetrhymena thermophila culture or in a solution containing the cilia of this organism, and subsequently subjected them to infection with Ichthyophthirius. As compared with the control, the trout pre-treated with Tetrahymena or its cilia showed a high degree of protection against lchthyophthirius infection. Similar experiments were reported by Goven, Dawe & Gratzek (1981) as well as Dickerson, Brown, Dawe & Gratzek (1984) who established protection in catfish against Ichthyophthirius by using fish-pathogenic Tetrahymena spp. as antigen. Biological control may lead to success especially if the specialists are sufficiently aware of the biocoenosis existing in the ponds. We know from the results of Sudarikov & Shigin (197.5) that certain members of the aquatic biocoenosis (molluscs, aquatic insects, copepods) may play an important role in eliminating the fish-parasitic Diplostomum cercariae. Palmieri, Cali & Heckman (1976) recommended a biological method against diplostomosis: they destroyed Diplostomum cercariae developing in snails using the hyperparasite Nosema strigeoidae. This procedure, although practical, is far from being realized yet. Keeping a systematic check on fish transportations and introductions constitutes an important part of parasite control. Transportations of useful and ornamental fishes for experimental purposes still take place without proper control, althougli the works of Hoffman et al., (1962), Bauer & Hoffman (1976) and Molnar (1984) have proved that the parasitoses currently causing the most severe problems are, almost without

324

K. Molnar

exception, a consequence of i&considered fish introductions. Unfavourabie experiences of fish introductions performed so far provide evidence that the veterinary documents certifying the parasite-free status of exported fishes and the qu~antine premises established in the recipient countries cannot prevent the spread of parasites. In the future, efforts should be made at restricting fish introductions to the importation of eggs and avoiding the feeding of fish larvae. It is much less compiicated and costly to maintain parasite-free status than to perform regular parasite control. SUMMARY The importance of parasitoses in freshwater, fish culture grows parallel with the development of fishbreeding. Especially in intensively cultured fish populations one has to reckon with outbreaks of parasitoses. Although parasite-related problems are different in cultures of salmonids, carp, tilapias, catfishes, eels and ornamental fish protozoan parasites are in general of greatest importance. Among protozoans, myxozoan parasites deserve attention as recent research on this group has brought several new results. Regarding the control of parasitic fish diseases, biological methods might be successful together with prevention and a broader scale of effective medicines. REFERENCES AMLACHER E. 1961. Die Wirkung

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FERCUSONH.W. & MCADAIR B. 1977. Protozoa associated with proliferative kidney disease in rainbow trout (Salmo gairdneri). Veterinary Record 100:158-159. GHITTINO P., ANDRUETTOS. & VIGLIANI E. 1977. L’amebiasi della trota iridea d’Allevamento. Rivistn Italiana di Piscicoltura e Ittiopatologia 12: 74-89.

GHITTINO P., SMITH F. & GLENN J.S. 1974. A case report Myxosporidia (Myxidium giardt) in the dermis of an American eel (Anguitta rostra&). Rivista Italiana di Piscicoltura e Ittiopatologia 9: 13-18. GOVEN B.A., DAWE D. L. & GRATZEK J.B. 1981. In vitro demonstration of serological cross-reactivity between Ichthyophthirius multifitiis Fouquet and Tetrahymena pyriformis Lwoff. Developmental and Comparative Immunology 5: 283-289. GRABDA J. & GRABDA E. 1966.Neguvon against carp dactylogyrosis (in Polish). Gospodarka rybnu 9: 5-6. GRATZEK J.B., GILBERT P., LOHR A.N., SHOTTS R.B. & BROWNJ. 1983. Ultraviolet light control of ~~k~hvoo~~tkjrjas ~ufti~iiis Fouquet in a closed fish culture recirculation system. ~o~r~luf of Fish Diseases 6: 145-153. . . HINE P.M. 1978. Variations in the spores of ~y~jdju~ zeu~andica~ Hine, 1975 (Protozoa: Myxosporidea). Nen Zealand Journal of Marine and Freskwafer Research 12: 189-195.

Freshwater fish parusites HINE P.M. 1980. A review of some species of Myxidium Butschli, 1882 (Myxosporodia: spp.). Journal of Protozoology 27: 260-267.

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HINTON M.J. & EVERSOLEA.G. 1979. Toxicity of ten chemicals commonly used in aquaculture to the black eel stage of the American eel. Proceedings of World Muriculture Society 10: 554-560. HOFFMAN G.L. 1974. Disinfection of contaminated water by ultraviolet irradiation, with emphasis on whirling disease (Myxosomu cerabralis) and its effect on fish. Transactions of the American Fisheries Society 103: 541-550. HOFFMAN G.L. 1976. Parasites of freshwater fishes. IV. Miscellaneous. The anchor parasite (Lernnea elegans) and related species. U.S. Fish and Wildlife Service, Fish Disease Leaflet 46: 8. HOFFMAN G.L. 1980. Parasitic diseases of laboratory fishes and their control. Synapse. Oficiul Public&ion of the American

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HOFFMAN G.L. 1983. Prevention and control of parasitic diseases of fishes. In: Parasites and parasitic diseases of fish. Abstract of papers for the 1st International Symposium of Ichthyoparasitology. Ceske Budejovice pp 38-39. HOFFMAN G.L., DUNBARC.E. & BRADFORDA. 1962. Whirling disease of trouts caused by Myxosoma cerebra/is in the United States. U.S. Fish and Wildlife Service, Special Scien& Report. Fisheries No. 427:.15. HOFFMAN G.L. & MEYER F.P. 1974. Parasites of freshwater fishes: a review of their control and treatment. T.F.H. Publications, Neptune, New Jersey. HOFFMAN G.L. & Pu-~z R.E. 1969. Host susceptibility and the effect of ageing, freezing, heat, and chemicals on spores of Myxosoma cerebralis. Progressive Fish-Culturist 31: 35-37. IMADA R. & MUROGA K. 1978. Pseudodactylogyrus microrchis (Monogenea) on the gills of cultured eels--II. Oviposition, hatching and development on the host. Bulletin of the Japanese Society of Scientific Fisheries 44: 571-576.

IMADA R. & MUROGA K. 1979. Pseudodactylogyrus microrchis (Monogenea) on the gills of cultured eels-III. Experimental control bv Trichlorfon. Bulletin of the Jaoanese Society of Scientific Fisheries 45: 25-29. KAN& T. & FUKUI H. 1982. Studies on Pleistopcora infection in eel, &Ula jabonicn I. Experimental induction of Microsporidiosis and Fumagillin efficacy. Fish Pathology 16: 193-200. KASAHARAS. 1962. Studies on the biology of the parasitic copepod Lernaea cyprinacea Linnaeus and the methods for controlling this parasite in fish culture ponds. Contributions of the Fisheries Laboratory, Fuculty of Agriculture, University of Tokyo 3: 103-196. (Eng. Synopsis). KENT M.L. & HEDRICKR.P. 1984. PKX, the causative agent of proliferative kidney disease (PKD) in Pacific Salmonid fishes and its affinities with the Myxozoa. Journal of Protozoology 31: 7. KHALIL L.F. 1971. The helminth parasites of African fresh water fishes. Part I: Zoogeographical affinites. La Revue de Zoologie et de Botanique Africaines 84: 236-263.

KOCYLOWSKIB., ZELAZNY I., ANTYCHOWICZI. & PANCYKJ. 1976. Incidence of carp coccidiosis

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Bulletin of Veterinary Institute, Pulawy 20: 12-17.

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