Acta vet. scand. 1995, 36, 283-298.

Parasite Infections in Danish Trout Farms

By K. Buchmann, A. Uldal and H. C. K. Lyholt

Department of Veterinary Microbiology, Section of Diseases, The Royal Veterinary and Agricultural Uni• versity, Frederiksberg, Denmark.

Buchmann, K., A. Uldal and H. Lyholt. Parasite infections in Dauish trout farms. Acta vet. scand. 1995, 36, 283-298. - Samples from 5 Danish freshwater trout farms rearing ( mykiss) were examined for parasite infections from Oc• tober 1993 until November 1994 and recorded parasites are listed. In addition, results from an examination of a mariculture net cage system are presented as well. A total of 10 metazoan and 10 protozoan parasites were recorded. The metazoans included Gy• rodactylus derjavini, salaris, Eubothrium crassum, Triaenophorus nodu• losus, Proteocephalus sp., Diplostomum spathaceum, Tylodelphus clavata and Argulus foliaceus from the freshwater farms. The protozoans Hexamita salmonis, lchthyobodo necator, lchthyophthirius multifiliis, Apiosoma sp., Epistylis sp., Trichodina nigra, T. mutabilis, T. fultoni, Trichodinella epizootica, and an lchthyophonus like intestinal par• asite were also detected in the freshwater trout farms. Based on lectin binding studies, few fish were found positive for the myxosporean parasite PKX although no clinical cases were reported. In the mariculture system, Lepeophtheirus salmonis and Caligus elongatus were found.

Rainbow trout; Oncorhynchus mykiss; meta:r.oans; protozoans; aquaculture.

Introduction The Danish production of rainbow trout (On• 1995) and more than 23 protozoan species corhynchus mykiss) has increased signifi• (Lorn & Dykova 1992) from this host. The ev• cantly during the last century from zero pro• ident importance of parasite infections in cul• duction in 1890 to a total annual output of tivated salmonids has resulted in a range of in• 42.000 metric tonnes (35.000 tonnes in fresh• vestigations on parasites of these . Thus water and 7.000 tonnes in sea water) in 1994. lists of parasites from salmonid farms and In order to optimize environmental and eco• hatcheries have previously been published nomical aspects of this aquacultural branch, a (Zitnan & Cankovic 1970, Hare & Frantsi research programme was implemented in 1974, McGuigan & Sommerville 1985). How• 1993. As a part of this programme we have ever, only a limited number of studies describ• monitored the parasite infections in selected ing the annual variations of all parasite types freshwater trout farms during 1 year. The in salmonid farms have been presented rainbow trout is the most important farmed (Wootten & Smith 1980, Rosengarten 1985, salmonid on world basis and has been trans• Poynton & Bennett 1985). The present paper planted into a large variety of habitats. This elucidates the annual variation of both meta• has resulted in the recording of more than 160 zoan and protozoan parasites from 5 trout different metazoan parasites (Buchmann et al. farms in Denmark.

Acta vet. scand. vol. 36 no. 3 - 1995 284 K. Buchmann et al.

Materials and methods in phosphate buffered 4% formaldehyde (pH A sample of 5 freshwater trout farms, all situ• 7.1) and tested for the presence of lectin (GS- ated in Jutland (western part of Denmark) 1 from Griffonia simplicifolia Sigma L-3759) with annual farm productions ranging from 50 binding PKX bodies using a modification of tonnes to 100 tonnes, were selected (Table the technique described by Hedrick et al. 1 a). (1992). Briefly, after an initial 20 min incuba• With few exceptions, monthly samples of 5 to tion with blocking buffer (5% BSA in TBS), 15 rainbow trouts (Oncorhynchus mykiss) biotinylated lectin in TBS (pH 8.0) (20 µg/ml) (stages O+ or 1 +) were taken from each of the was added to the smears and reacted for 120 farms (Table 1 b ). The fishes were examined min. The smears were subsequently rinsed (5 immediately or brought to the laboratory min) in TBS and incubated with avidin and bi• under refrigerated conditions and examined otin conjugated alkaline phosphatase in TBS within 24h. All organs including fins, gills, with 2.5% BSA. Fast Red substrate system skin, eyes, body cavity, heart, liver, spleen, tablets (DAKO) (in Tris-HCl, pH 8.2) was kidney, swim bladder, oesophagus, stomach, used as chromogen. Histology sections of kid• pyloric caeca, and intestine were examined. ney and spleen from an infected trout served The investigation was performed with a dis• as positive control. Positive parasite cells ap• secting microscope (magnification 10-40 x) peared bright red. and with smear or squash preparations in For identification of trichodinids, skin mucus compound microscopes (magnification 100- smears containing parasites from trout were 1000 x). On few occasions, mucus scrapings prepared on slides and incubated for 20 min from body surface and fins of spawners were with 2% AgN03, exposed to UV-light for 10 examined for Gyrodactylus parasites. min and subsequently mounted in DePex lip• Kidney smears on slides were prepared, fixed ofilic embedding medium.

Table 1 a. Trout farms examined for parasite infections from October 1993 until November 1994.

Farm Water source Production Location

1 Stream water/well water Fry/fingerlings Connected to other farms 2 Stream water/well water Fry/fingerlings/consumption fish Isolated from other farms 3 Lake water Consumption fish Connected to other farms 4 Stream water/well water Fingerlings/consumption fish Connected to other farms 5 Stream water Fingerlings/consumption fish Connected to several farms

Table 1 b. Number of rainbow trouts from the 5 fish farms in the respective monthly samples.

1993 1994 Farm Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov

1 0 11 0 11 13 10 10 10 7 5 10 7 2 8 2 0 0 0 0 5 10 10 10 10 9 6 6 7 5 3 15 10 0 11 10 9 8 10 10 6 6 7 5 6 4 0 0 10 0 5 10 0 5 10 5 5 7 7 6 5 0 0 0 10 0 10 10 5 10 7 5 10 8 7

Acta vet. scand. vol. 36 no. 3 - 1995 Parasite infections in Danish trout 285

Table 2. Parasites recorded in rainbow trout (Oncorhynchus mykiss) in 5 Danish farms from October 1993 until November 1994.

Parasite Authority Location in host Farm recorded

Protozoans: Hexamita salmonis Moore 1923 Intestine, pyloric caeca 1, 2, 3, 4, 5 Ichthyobodo necator Henneguy 1884 Gills, fins, skin 1, 4 lchthyophthirius multifiliis Fouquet1876 Fins and skin 3,4,5 Trichodina fultoni Davis 1947 Skin 2 Trichodina nigra Lorn 1961 Skin 1, 3, 4, 5 Trichodina mutabilis Kazubski & Migala 1968 Skin 1,3,4,5 Trichodinella epizootica Raabe 1950 Gills 5 Apiosoma sp. Blanchard 1885 Fins and skin 1,2,3,4,5 Epistylis sp. Ehrenberg 1830 Fins and skin 1,2,3,4,5 PKX Kidney 1,3,4,5 Unknown taxonomic affiliation: lchthyophonus like organism Anterior intestine 1,2,3,4,5

Metazoans: Gyrodactylus derjavini Mikailov 1975 Fins and skin 1,3,4,5 (Malmberg et Malmberg 1987) Gyrodactylus salaris Malmberg 1957 Fins and skin 1, 5 Cestoda Eubothrium crassum Bloch 1979 Juveniles in pyloric caeca and intestine 3 Triaenophorus nodulosus Pallas 1819 Juveniles in body cavity 3 Proteocephalus sp. Weinland 1858 Juvenile in intestine 3 Digenea Diplostomum spathaceum Rudolphi 1819 Metacercaria in lens 3,5 Tylodelphus clavata Nordmann 1832 Metacercaria in vitreous humour 3 Crustacea Argulus foliaceus Linnaeus 1758 Skin 3 Lepeophtheirus salmonis Kr!>lyer 1837 Skin, mariculture only Caligus elongatus Nordmann 1832 Skin, mariculture only

Snails inhabiting the eyefluke infected trout 70% ethanol or 4% phosphate buffered for• farm were collected in the fish ponds in Au• maldehyde and mounted in glycerine gelatine gust 1994. They were placed at room temper• or ammonium picrate/glycerine (Malmberg ature in 40 ml vials containing 20 ml pond wa• 1957) for identification. ter and monitored for cercarial shedding during the following 48h. Results Crustacean ectoparasites from large speci• The recorded parasites and their location in mens of rainbow trout (> 300 g) originating the hosts are presented in Table 2. from a high salinity mariculture net cage system were collected as well during August Metazoan parasites 1993. Monogeneans. Only 2 species ofmonogen• Collected metazoan parasites were fixed in eans, Gyrodactylus derjavini (Fig. 1) and Gy-

Acta vet. scand. vol. 36 no. 3 - 1995 286 K. Buchmann et al.

Figure 1. Gyrodactylus derjavini from a Danish rainbow trout (Farm 5, March 1994). Mounted in ammonium picrate/glycerine (Malmberg 1957). Scale bar: 10 µm. For recording of Figs. 1 and 2 a Leitz DMRBE microscope equipped with interference contrast with polarisation (anchors) or phase contrast (marginal hooklets) was used for magnification. A digital image processing and analysis system (Leica QSOO MC, Leica Cambridge Ltd, Eng• land) was applied for recording. (Courtesy of Dr. G. Malmberg, University of Stockholm). rodactylus salaris (Fig. 2), were detected. Cestodes. Cestodes were found exclusively However, the species recorded as G. derjavini in the farm receiving water from a natural in Farm 5 in August 1994 deviated slightly lake (Farm 3). Infection in autumn and winter from the type specimen by having a slightly (prevalence 0-40% ), intensity of infection 1 broader ventral bridge (G. Malmberg, per• parasite per infected host) with Eubothrium sonal comm.). One farm (Farm 2) was not crassum, Proteocephalus sp., Triaenophorus found infected with gyrodactylids (fry and fin• nodulosus, was found. Only single species in• gerlings ). Two farms harboured G. derjavini fections were recorded. only (Farm 3 and 4), and Farm 1 was exclu• Digeneans. No adult trematodes were sively infected with G. safaris except for No• found. Only metacercariae of the eye flukes vember 1994 where both species were found. Diplostomum spathaceum (located in the In Farm 5, the winter and early spring infec• lens) and Tylodelphus clavata (located in the tion with G. salaris was replaced by G. derja• vitreous humour) were recorded. Both spe• vini in late May (Table 3). cies occurred in Farm 3, whereas only a slight

Acta vet. scand. vol. 36 no. 3 - 1995 Parasite infections in Danish trout 287

.. s&111Ms;Oen111

Figure 2. Gyrodactyfus safaris from a Danish rainbow trout (Farm 5, May 1994). Scale bar: 10 µm.

D. spathaceum infection was found in Farm 5 Farm 3, a slight seasonal variation of the (10% prevalence in January and 20% in abundantly occurring D. spathaceum with April; no infection in the other months). In lower prevalence from April until June was

Table 3. Occurrence of Gyrodactyfus safaris and G. derjavini on rainbow trout in 4 Danish trout farms "(Farm 1, 3, 4, 5) from October 1993 until November 1994. Farm 2 was not infected.

1993 1994 Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sept Oct Nov

G. 1 5 5 5 1* 1* 1* salaris G.de 5 4 5 3 3 3 rjavini l*

*: G. salaris was found on spawners only.

Acta vet. scand. vol. 36 no. 3 - 1995

Parasite infections in Danish trout 289

Prevalence Mean intensity 100 1 ------6

Month

D Prevalence - Intensity

Figure 4. Seasonal variation of Tylodelphus clavata infections (prevalence and mean intensity) in Farm 3 from October 1993 until November 1994.

Farm 4 was found lectin-positive in May only, Okamoto et al. (1985) was found throughout Farm 5 fish showed reaction in May, in July, the year in relatively low prevalences (Fig. 7). and September, Farm 3 was positive in May, The organisms were located in the anterior in• June, July, and Farm 1 in June only. testinal wall or intestinal content, which often Ciliates. /chthyophthirius multifiliis oc• was of a yellowish jelly like consistence in in• curred irregularly on the fins and skin of fishes fected fish. from 3 farms. No infection was found in Trichodina spp. occurred frequently but in Farms 1and2. In Farm 3, 14% were infected low numbers on the trout skin thoughout the in September only, in Farm 5, 25% were in• year (Fig. 8). T. nigra and T. mutabilis was fected in October, and in Farm 4 this ciliate found. In addition, in Farm 2 another species was found in August ( 40% ), September with a diameter of the adhesive disc of speci• (14%) and October (14% ). mens stained with silver nitrate was measured Apiosoma sp. and Epistylis sp. were found to 74-80 µm, the number of denticles were 29, sporadically and infrequently on the skin and and the number of radial pins per denticle fins of trout throughout the year. blade was 14. The center of the disc was un• /chthyophonus-like protistan. An intestinal stained with argentophilic granules. These -like organism with an appearance as characteristics and the overall shape of the /chthyophonus-stages (Fig. 6) described by denticles suggested a species determination as

Acta vet. scand. vol. 36 no. 3 - 1995

Parasite infections in Danish trout 291

Figure 6. Ichthyophonus like unicellular intestinal organism. Dividing form at the right. Scale bar: 20 µm. is extremely susceptible to this mono• tance. Cestodes of the Proteocephalus genean (Bakke & MacKenzie 1993). In con• in Danish trouts were previously reported by trast the Baltic Neva strain of the same host From & H¢rlyck (1981) and later identified species are relatively resistant to this parasite by Hanzelova & Scholz (1992) as Proteoceph• (Bakke et al. 1990). Before any conclusions alus neglectus. This paper is the first record of are drawn on the importance of G. safaris in• Triaenophorus nodulosus in Denmark. This fections of Danish rainbow trout for the cestode has pike (Esox Lucius) as final host, spread of the parasite to different salmon and the life cycle of this parasite probably oc• stocks, controlled experiments should eluci• curs in the natural lake connected to the farm. date the effect of the isolated Danish strain of Eubothrium crassum is a well known parasite G. safaris on various strains of Sa/mo salar. of rainbow trout (Wootten 1972, Buchmann et al. 1995) and was found in Sa/mo trutta in Cestodes Denmark (Buchmann 1987). However, this is Only 1 farm (which received natural lake wa• the first report of this cestode in Danish rain• ter) was found infected with cestodes. Eu• bow trout. Whether trout in this farm are in• bothrium crassum, Proteocephalus sp. Uuve• fected through ingestion of copepods acting as nile) and Triaenophorus nodulosus were intermediate hosts or due to eating transport found in low graded infections in autumn and hosts like sticklebacks (2 possible infection winter. Cestodes of these genera are known routes indicated by Vik (1963)) is not yet pathogens of salmonids (Bauer & Solomatova known. However, the infected farm received 1984, Engelhardt et al. 1988, Berland 1991). water from a natural lake and it is supposed However, the very low infection level found in that infective stages in intermediate hosts (co• the Danish farm is probably of minor impor- pepods) entered the farm via the inlet water.

Acta vet. scand. vol. 36 no. 3 - 1995

Parasite infections in Danish trout 293

Figure 8. Micrographs of a) Trichodina nigra, b) T. mutabilis and c) T. fultoni from Danish rainbow trout farms.Scale bar: 20 µm.

1986 b). This will explain the observed de• 1974, Buchmann et al. 1995) and never before crease in prevalence of infection during win• from Danish rainbow trout. The situation in ter and early spring. Uninfected fish intro• the present farm should be followed, as Onco• duced into the farm during that season (which rhynchus mykiss seems to be quite susceptible is common practice) are exposed to a reduced to infection. Thus devastating infections with infection pressure which will result in the ob• Argulus foliaceus on rainbow trout (several served decrease in farm infection. The infec• hundred specimens per host) were found in a tion with Tylodelphus clavata was very low put and take Jake (stocked with trout for an• and is probably of minor importance. Diplos• gling purposes) on the Danish island of Born• tomum metacercariae located in the lens of holm in the Baltic in August 1992 (Buchmann, rainbow trout have been shown to cause cata• unpublished). ract (Shariff et al. 1980), affect growth of the The salmon lice, Lepeophtheirus salmonis and host (Sato et al. 1976, Buchmann & Uldal Caligus elongatus, are well known pathogens 1994) and even elicit mortality of smaller in cage rearing of salmonids (Wootten et al. hosts (Brassard et al. 1982). Thus it is possible 1982) and the finding of these crustaceans that the infection in Farm 3 will influence the suggests that parasite investigations on rain• fish production. bow trout in net cage rearing enterprises should be reinforced. Crustaceans Intestinal trematodes, nematodes and acan• The branchiuran Argulus foliaceus was only thocephalans were not found in rainbow trout detected once in 1 farm (Farm 3) receiving in the present investigation although some of lake water to the ponds. Therefore it is likely these groups are quite common in feral trout that larval stages enter the farm with inlet wa• in Denmark (Buchmann 1989). This lack of ter from the natural Jake. This parasite is a se• parasites which demand ingestion of interme• rious pathogen in fish farming enterprises diate hosts as insect larvae or crustaceans cor• (Bauer et al. 1973) but has not been reported responds to the sparcity of similar parasites in frequently from the rainbow trout (Kennedy cultured salmon (Wootten & Smith 1980). It

Acta vet. scand. vol. 36 no. 3 - 1995 294 K. Buchmann et al.

can be explained by the sparce and unvaried ellate numbers in the anterior part of the fauna in intensive trout ponds whereby appro• intestine. However, already Moore (1925) priate intermediate host are lacking. Previ• stated that this part is preferably infected in ously, marine nematodes occurred in Danish the earliest state of the infection whereafter freshwater trout (Christensen & From 1978) the parasite spreads to the rest of the intes• due to feeding with marine fish offals contain• tine. ing nematode larvae. As this practice is pres• /chthyobodo necator. The ectoparasitic kinet• ently prohibited and trout exclusively are fed oplastid flagellate occurred infrequently on with pelleted dry feed the Danish trout should the exterior part of the trout. Although this be considered free from anisakid nematodes. parasite is a known pathogen of salmonids eliciting host mortality (Christensen et al. Protozoans 1963, Robertson 1979) the low infection found Hexamita salmonis. The intestinal di• in the present study did not allow a closer plomonadid flagellate Hexamita salmonis was analysis. early recognized as a serious pathogen in sal• /chthyophthirius multifiliis. Trophonts of this monids (Moore 1925). However, the pathoge• ciliate producing white spot disease in fish nicity of the protozoan to some salmonids was (Bauer et al. 1973) occurred sporadically and later disputed by Uzman et al. (1965) although was associated with fry morbidity and mortal• these authors found a negative effect on the ity in Farm 4 (fish farmers information). rainbow trout health of experimental infec• Larger fish were found to harbour few speci• tions. In our study we registered considerable mens without showing signs of weakness. This fry mortality in the most heavily Hexamita in• might be explained by manifestations in the fected farm (Farm 1) and experiments are in fishes of resistance mechanisms to this ciliate progress for evaluation of the pathogenicity of (Hines & Spira 1974). However, the frequent the Danish parasite strain to the Danish rain• use of chloramine, formaldehyde and copper bow trout. sulphate in the ponds may have influenced the Hexamita salmonis has previously been re• parasite abundance. ported from European rainbow trout farms The trichodinids Trichodina nigra, T. mutabi• (Christensen et al. 1963, Zitnan & Cankovic lis and T. fultoni and sessile ciliates as Apios• 1970, Ferguson 1979, Rosengarten 1985, Poyn• oma sp. and Epistylis sp. occurred throughout ton & Bennett 1985, Poynton 1986). We found the year but not as abundantly as similar cili• that mostly fry and smaller fingerlings are in• ate types reported by Wootten & Smith (1980) fected which is in accordance with Rosen• in salmon hatcheries. This might be due to the garten (1985) and Poynton (1986). The pres• frequent use of chloramine, formaldehyde ence of the parasite in all seasons suggests that and copper sulphate in the farms. The effect Hexamita salmonis has a wide temperature of these parasites on the Danish trout produc• amplitude for reproduction although this has tion is not yet clear. not been experimentally demonstrated. The PKX. The low prevalence and sporadic oc• location of this flagellate along the entire currence of this parasite in the examined length of the fry intestine in heavily infected farms was only detected by the lectin-binding fish is worth noting. That this location is due technique on smears and further studies to some intraspecific competition is indicated should evaluate the reliability of this tech• as lightly infected fish harboured higher flag- nique. PKX was recorded for the first time in

Acta vet. scand. vol. 36 no. 3 - 1995 Parasite infections in Danish trout 295

Denmark in 1982(Olesen1985) and the infec• pathogenicity, be followed during the follow• tion is considered a serious obstacle to trout ing years. Also Ichthyophthirius multifiliis is a farming (Clifton-Hadley et al. 1984, Hedrick known pathogen and requires studies on pro• 1993). However, the impact of this parasite on phylaxis and treatment. The record of the sal• the trout production in the examined Danish mon lice in Danish mariculture systems calls trout farms is not clear. for further investigations of parasite infec• The fungus like organism with an Ichthyopho• tions in those enterprises. nus-like appearance recorded in the intestines of fish from the Danish trout farms call for further investigations. Their , life Acknowledgements Agricultural cycle and possible pathogenicity has not yet This work was supported by the Danish and Veterinary Research Council and is a part of the been elucidated. However, a similarity was Danish programme on Disease prevention, genetics found to certain stages of Ichthyophonus ho• and nutrition in rainbow trout production. The au• feri cultivated by Okamoto et al. (1985). In vi• thors are indebted to Steen M!llller (National Insti• tro cultivation of these recovered parasites tute of Science, Tjele), Jon From (Inland Laboratory, Silkeborg), Viggo H!llrlyck, be implemented and compared to the should Christian Graver, Per Aarup (Danish Trout Culture Japanese studies. Research Station, Br!llns) and T. Nielsen (Brande), who collected a considerable number of Conclusions the examined fishes. Sincere thanks go to Dr. Goran The number of trout farms in Denmark is ex• Malmberg (University of Stockholm) who kindly guided K. Buchmann into the Gyrodactylus taxon• ceeding 400. Therefore this report on para• omy and determined or verified our determination sites in Danish trout-rearing enterprises is not of Gyrodactylus species. The cooperation of Dr. Ken claiming to be representative of all Danish MacKenzie (Marine Laboratory, Aberdeen) is like• farms. Other parasite types might be found wise appreciated. Dr. N.J. Olesen (National Veteri• Laboratory, Arhus) provided instructions on during extended surveys in Danish trout nary the modified lectin binding assay. farms. Also the time delay between collection of fish and examination may influence the re• sults. However, a number of parasite prob• References lems have been pinpointed. Of these infec• Bakke TA, MacKenzie K: Comparative susceptibil• tions with the monogeneans Gyrodactylus ity of native Scottish and Norwegian stocks of derjavini and G. salaris warrant detailed stud• , salar L., to Gyrodactylus salaris Malmberg: Laboratory experiments. Fish. biology and pathology in ies on population Res. 1993, 17, 69-85. different salmonid hosts. The diplostomid Bakke TA, Jansen PA, Hansen LP: Differences in the trematode infections are prevalent at least in host resistance of Atlantic salmon, Salmo salar L., some farms and require further research on stocks to the monogenean Gyrodactylus salaris prophylaxis and treatment. The intestinal Malmberg, 1957. J. Fish Biol. 1990, 37, 577-587. Bakke TA, Janssen PA, Kennedy CR: The host spec• flagellate Hexamita salmonis is often found ificity of Gyrodactylus salaris Malmberg (Platy• associated with fry mortality and morbidity. helminthes, Monogenea): susceptibility of Onco• Future experiments should elucidate the pos• rhynchus mykiss (Walbaum) under experimental sible pathogenicity of this parasite and pro• conditions. J. Fish Biol. 1991, 39, 45-57. Solomatova VP: The cestode Trianoph• vide prophylactic measures. The detection, Bauer ON, orus crassus (Pallas) (Pseudophyllidea: Triaeno• epidemiology and importance of PKD in phoridae) as a pathogen of cage-reared salmon• Danish trout farms should, due to its possible ids. J. Fish Dis. 1984, 7, 501-504.

Acta vet. scand. vol. 36 no. 3 - 1995 296 K. Buchmann et al.

Bauer ON, Musselius VA, Strelkov Yu A: Bolezni bow trout fry Salmo gairdneri Richardson. J. Fish Prudovykh ryb. Izdatel stro »Kolos« Moskva Dis. 1979, 2, 57-67. 1969. (Diseases of pond fishes). Israel program From J, H¢rlyck V.· First recorded occurrence of for scientific translations, Jerusalem 1973. Proteocephalus percae (Millier, 1780) in Danish Berland B: Cestoda, Bendelmark. (Cestodes, tape• farmed trout. Bull. Eur. Ass. Fish Pathol. 1981, 1, worms). In: Poppe TI (Ed) Fiskehelse (Fish 40-41. Health). John Grieg Forlag 1991. Hanzelova V, Scholz T: Redescription of Proteo• Buchmann K: Cestodes of migratory trout (Salmo cephalus neglectus La Rue, 1911 (Cestoda: Pro• trutta L.) from the Baltic Sea. Bull. Eur. Ass. Fish teocephalidae ), a trout parasite, including desig• Pathol. 1987, 7, 115-117. nation of its lectotype. Folia Parasitol. 1992, 39, Buchmann K: Trematodes and acanthocephalans of 317-323. Salmo trutta from the Baltic sea. Bull. Eur. Ass. Hare GM, Frantsi C: Abundance and potential pa• Fish Pathol. 1989, 9, 9-11. thology of parasites infecting salmonids in Cana• Buchmann K, Uldal A: Effects of eyefluke infections dian maritime hatcheries. J. Fish Res. Board on growth of rainbow trout (Oncorhynchus my• Canada 1974, 31, 1031-1036. kiss) in a mariculture system. Bull. Eur. Ass. Fish Hedrick RP, MacConnell E, de Kinkelin, P: Prolife• Pathol. 1994, 14, 104-107. rative kidney disease of salmonid fish. Annual Buchmann K, Uldal A, Lyholt HCK: A checklist of Rev. Fish Dis. 1993, 277-290. rainbow trout metazoan parasites. Acta vet. Hedrick RP, Marin M, Castagnaro M, Monge D, de scand. 1995, 36, 295-314. Kinkelin P: Rapid lectin based staining proce• Brassard P, Rau ME, Curtis MA: Infection dynamics dure for the detection of the myxosporean caus• of Diplostomum spathaceum cercariae and para• ing proliferative kidney disease in salmonid fish. site-induced mortality of fish host. Parasitology Dis. aquat. Org. 1992, 13, 129-132. 1982, 85, 489-493. Hines RS, Spira DT: Ichthyophthiriasis in the mirror Christensen NO, Jensen M, Rasmussen CI: Fish dis• carp Cyprinus carpio (L.) V. Vet. J. Fish Biol. eases in Denmark. Bull. Off. int. Epiz. 1963, 59, 1974, 6, 373-378. 21-29. Hoglund, J., Thulin, J.: Identification of Diplosto• Christensen S, From J: Rundorme og deres bekrem• mum spp. in the retina of perch Perea fluviatilis pelse hos dambrugsfisk. (Roundworms and their and the lens of roach Rutilus rutilus from the Bal• eradicaton in farmed fish). Ferskvandsfiskeribla• tic Sea - an experimental study. Syst. Parasitol. det 1978, 8, 94-100. 1992, 21, 1-19. Clifton-Hadley RS, Bucke D, Richards RH: Prolife• Johnsen BO, Jensen Al: Introduction and establish• rative kidney disease of salmonid fish: a review. ment of Gyrodactylus salaris Malmberg, 1957, on J. Fish Dis. 1984, 7, 363-377. Atlantic salmon, Salmo salar L., fry and parr in Cone DK, Odense PH: Pathology of 5 species of Gy• the River Vefsna, northern Norway. J. Fish Dis. rodactylus Nordmann, 1832 (Monogenea). Can. 1988, 11, 35-45. J. Zoo!. 1984, 62, 1084-1088. Kennedy CR: A checklist of British and Irish fresh• Engelhardt A, Mirle C, Granitza I, Petermann H: water fish parasites with notes on their distribu• Untersuchungen zum Vorkommen, zur Schad• tion. J. Fish Biol. 1974, 6, 613-644. wirkung und Bekampfung von Proteocephalus Lorn J, Dykova I: Protozoan parasites of fishes. De• neglectus bei Regenbogenforellen in der Netz• velopments in aquaculture and fisheries science, kafighalten. (An investigation into the the occur• Elsevier. 1992, 26, 1-315. rence, pathology and control of Proteocephalus Madhavi R, Anderson RM: Variability in the suscep• neglectus infections in rainbow trout in net tibility of the fish host Poecilia reticulata to infec• cages). Monatshefte fiir Veterinarmedizin 1988, tion with Gyrodactylus bullatarudis. Parasitology 43, 169-172. 1985, 91, 531-544. Ergens R: Gyrodactylus from Eurasian freshwater Malmberg G: Om forekomsten af Gyrodactylus pa and Thymallidae. Folia Parasitol. svenske fisk (On the occurrence of Gyrodactylus 1983, 30, 15-26 on Swedish fishes). Skr. sodr. Sver. Fisk. For. Ferguson HW: Scanning and transmission electron Arsskr. 1957, 1956, 19-76. microscopical observations on Hexamita salmo• Malmberg G: Gyrodactylus infestations on species of nis (Moore, 1922) related to mortalities in rain- Salmo in Danish and Swedish hatcheries. Norw.

Acta vet. scand. vol. 36 no. 3 - 1995 Parasite infections in Danish trout 297

J. Zoo!. 1973, 21, 325-326. gebiet Fischkrankheiten und Fischhaltung der Malmberg G: and gyrodactylosis of Tierarztlichen Hochschule Hannover, Germany salmonidae. Bull. Fr. Peche Piscic. 1993, 328, 5- 1985. 46. Sato T, Hoshina T, Horiuchi M: On worm cataract of Malmberg G, Malmberg M: Gyrodactylus in salmon rainbow trout in Japan. Bull. Jap. Soc. Sci. Fish. and rainbow trout farms. In: Stenmark A, Malm• 1976, 42, 249. berg G (Eds): Parasites and diseases in natural Shariff M, Richards RH, Sommerville C: The histo• waters and aquaculture in Nordic countries. Na• pathology of acute and chronic infections of rain• turhistoriska Riksmuseets Reprocentral, Stock• bow trout, Sa/mo gairdneri Richardson with eye holm. 1987, 199-204. flukes, Diplostomum spp. J. Fish Dis. 1980, 3, McGuigan JB, Sommerville C: Studies on the effects 455-465. of cage culture of fish on the parasite fauna in a Sous SM: Influence of abiotic factors on emission lowland freshwater loch in the west of Scotland. and survival of cercariae of Diplostomum Z. Parasitenk. 1985, 71, 673-682. chromatophorus (Brown, 1931) (, Di• Mo TA: Variations of opisthaptoral hard parts of Gy• plostomidae). Ecol. Parasitol. 1992, 1, 154-159. rodactylus safaris Malmberg, 1957 (Monogenea: Stables JN, Chappell LH a: The epidemiology of di• Gyrodactylidae) on rainbow trout Oncorhyn• plostomosis in farmed rainbow trout from north• chus mykiss (Walbaum, 1792) in a fish farm, with east Scotland. Parasitology 1986, 92, 699-710. comments on the spreading of the parasite in Stables JN, Chappell LH b: Diplostomum spatha• south-eastern Norway. Syst. Parasitol. 1991, 20, ceum (Rud. 1819): Effects of physical factors on 1-9. the infection of rainbow trout (Sa/mo gairdneri) Moore E: Octomitus salmonis, a new species of intes• by cercariae. Parasitology 1986, 93, 71-79. tinal parasite in trout. Trans. Amer. Fish. Soc. Vzmann JR, Paulik GJ, Hayduk SH: Experimental 1925, 54, 74-93. hexamitiasis in juvenile ( Oncorhyn• Olesen NJ: PKD i 1984 (PKD in 1984). Ferskvands• chus kisutch) and steelhead trout (Sa/mo gaird• fiskeribladet 1985, 5, 126-129. neri). Trans. Amer. Fish. Soc. 1965, 94, 53-61. Okamoto N, Nakase K, Suzuki H, Nakai Y, Fujii K, Vik R: Studies of the helminth fauna of Norway. IV. Sano T: Life history and morphology of Ichthyo• Occurrence and distribution of Eubothrium cras• phonus hoferi in vitro. Fish Pathol. 1985, 20, 273- sum (Bloch, 1779) and E. salvelini (Schrank, 285. 1790) (Cestoda) in Norway, with notes on their Poynton SL: Distribution of the flagellate Hexamita life cycles. Nyt Mag. Zoo!. 1963, 11, 47-73. salmonis Moore, 1922 and the microsporidian Wootten R: Occurrence of Eubothrium crassum Loma salmonae Putz, Hoffman and Dunbar, (Bloch, 1779) (Cestoda: Pseudophyllidea) in 1965 in brown trout, Sa/mo trutta L., and rainbow brown trout, Sa/mo trutta L., and rainbow trout, trout, Sa/mo gairdneri Richardson, in the River S. gairdneri Richardson, 1836, from Hanning• ltchen (U.K.) and 3 of its fish farms. J. Fish Biol. field Reservoir, Essex. J. Helminthol. 1972, 46, 1986, 29, 417-429. 327-339. Poynton SL, Bennett CE: Parasitic infections and Wootten R, Smith JW· Studies on the parasite fauna their interactions in wild and cultured brown of juvenile Atlantic salmon, Sa/mo salar L., cul• trout and rainbow trout from the river ltchen, tured in fresh water in eastern Scotland. Z. Para• Hampshire. In: Ellis AE (ed): Fish and Shellfish sitenk. 1980, 63, 221-231. Pathology. Academic Press, London. 1985, 353- Wootten R, Smith JW, Needham EA: Aspects of the 357. biology of the parasitic copepods Lepeoph• Robertson DA: Host parasite interactions between theirus salmonis and Caligus elongatus on Ichthyobodo necator (Henneguy, 1883) and farmed salmonids, and their treatment. Proc. farmed salmonids. J. Fish Dis. 1979, 2, 481-491. Royal Soc. Edingb. (B) 1982, 81, 185-197. Rosengarten R: Parasitologische Untersuchungen an Zitnan R, Cankovic M: Comparison of the epizooto• Regenbogenforellen (Sa/mo gairdneri Richard• logical importance of the parasites of Sa/mo son) in einer Forellenteichwirtschaft in Nieder• gairdneri irideus in the 2 coast areas of Bosna and sachsen. (Parasitological investigations on rain• Herzegovina. Helminthologia 1970, 11, 161-166. bow trout (Sa/mo gairdneri Richardson) in a trout farm in Niedersachsen) Dissertation. Fach-

Acta vet. scand. vol. 36 no. 3 - 1995 298 K. Buchmann et al.

Sammendrag derne Eubothriurn crassurn, Proteocephalus sp., Tri• Parasitinfektioner i danske ¢rredbrug. aenophorus nodulosus, trematoderne Diplostornurn spathaceurn og Tylodelphus clavata, krebsdyrene Ar• Regnbue(llrreder fra 5 danske ferskvandsdambrug er gulus f oliaceus, Lepeophtheirus salrnonis og Caligus blevet underkastet en parasitologisk unders(llgelse elongatus. fra oktober 1993 til november 1994. Desuden er ek• De encellede parasitter omfatter Hexarnita salrno• toparasitter fra et havbrugssystem med regnbue• nis, lchthyobodo necator, lchthyophthirius rnultifiliis, (llrreder blevet registreret. Ved unders(llgelsen er der Apiosorna sp., Epistylis sp., Trichodina nigra, T. rnu• blevet fundet 10 arter af flercellede snyltere samt 10 tabilis, T. fultoni, Trichodinella epizootica og PKX. encellede snyltere. De flercellede omfatter monoge• Desuden er der i enkelte regnbue(llrreders tarm re• nerne Gyrodactylus safaris og G. derjavini, cesto- gistreret en Ichthyophonus lignende organisme.

(Received November 30, 1994; accepted April 29, 1995).

Reprints may be obtained from: K. Buchmann, Department of Veterinary Microbiology, Section of Fish Dis• eases, Royal Veterinary and Agricultural University, 13 Biilowsvej, DK-1870 Frederiksberg C, Denmark.

Acta vet. scand. vol. 36 no. 3 - 1995