FOLIA PARASITOLOGICA 46: 179-184, 1999

Transmission of the monogenean Gyrodactylus salaris

Arnulf Soleng1, Peder A. Jansen2 and Tor A. Bakke1

1Zoological Museum, University of Oslo, Sars gate 1, N-0562 Oslo, Norway; 2Department of Zoology, Norwegian University of Science and Technology, N-7034 Trondheim, Norway

Key words: Gyrodactylus salaris, Monogenea, temperature, transmission, Salmo salar

Abstract. The present study is focusing on the transmission of the monogenean ectoparasite Gyrodactylus salaris Malmberg, 1957, a major pathogen on natural populations of Norwegian Atlantic salmon, Salmo salar L. In laboratory experiments the transmission rate of G. salaris after direct host to host contact was positively correlated with water temperature (1.2, 4.7 and 12.2°C). The transmission of detached G. salaris in the planktonic drift was studied in field experiments where salmon parr were individually isolated for 24 hours in small wire mesh cages suspended in the water column. Ten out of 157 salmon parr (prevalence 6.4%, mean intensity 1.0) contracted G. salaris infections after this exposure. Furthermore, 200 uninfected marked salmon parr were released into the same area of the river. After 24 and 48 hours, respectively 18 and 19 marked parr were caught by electro-fishing. The prevalence of G. salaris was 44.4% (mean intensity 1.9) after 24 hours, rising to 57.9% (mean intensity 2.3) after 48 hours. Gyrodactylids have no specific transmission stage or swimming ability, but detached G. salaris drifting in the water column were found to infect salmon parr. However, the transmission rate was markedly higher to free-living fish, suggesting that transmission routes such as indirect transmission from the substrate or direct contact transmission from infected live and/or dead fish, are relatively more important than transmission by drifting detached parasites.

Gyrodactylid monogeneans are viviparous, posses- investigate parasite transmission to caged salmon parr sing no specific transmission stage or swimming ability. exposed only to detached G. salaris drifting in the river Thorough knowledge about the transmission of these water, and compare this to parasite transmission to monogenean ectoparasites is scarce, but four different marked and released parr swimming freely in the river. routes are listed by Bakke et al. (1992): (1) contact with living infected fishes; (2) contact with detached MATERIALS AND METHODS parasites on the substrate; (3) contact with infected dead fishes; and (4) contact with detached parasites drifting The laboratory experiments were performed at the in the water column. It is generally agreed that gyro- Zoological Museum in Oslo, while the field experiments were dactylids transmit after direct host contact (Bychowsky carried out in the River Glitra, a tributary to the River Lierelva 1957, Malmberg 1957, Bauer 1958, Scott and Anderson in Buskerud County, southeast Norway. All fish used were 1984, Kamiso and Olson 1986). However, Atlantic hatchery reared Atlantic salmon parr (age 1+) of the River salmon, Salmo salar L., parr are territorial (Kalleberg Lierelva stock ranging from 6 to 10 cm in fork length, 1958, Keenleyside 1962, Folmar and Dickhoff 1980), previously not exposed to any gyrodactylid infections. The Gyrodactylus salaris strain used in the laboratory experiments and rarely have direct contact (Keenleyside 1962), originated from infected wild salmon parr electro-fished in the indicating the importance of indirect transmission routes River Lierelva approximately one month prior to the start of for gyrodactylids parasitising this host species. Bakke et the experiments. The parasitological terms used follow the al. (1992) suggested that the ability of detached definitions given in Margolis et al. (1982). parasites in the drift to re-infect fishes may have been underestimated. The effect of ambient water The effect of water temperature on the transmission rate temperature on gyrodactylid transmission rates is poorly of G. salaris – laboratory experiments The experiments were performed at three different studied, although Bakke et al. (1991) reported a positive temperatures: 1.2°C (range 1.1-1.3), 4.7°C (range 4.5-4.9°C) corre-lation between temperature and transmission of and 12.2°C (range 11.5-12.9°C). The experiments at 1.2°C Gyro-dactylus salaris Malmberg, 1957 from salmon were performed in a refrigerated room, while the other parr to a potential transport host, the European eel, experiments were performed in a fish holding laboratory. We Anguilla anguilla (L.). used grey plastic boxes (37 × 23 × 10 cm) with wire mesh The aim of the present study was to elucidate, in bottom (mesh size 0.5 × 0.5 cm) in all experiments. In the laboratory experiments, the effects of water temperature experiments in the fish holding laboratory the boxes were on the transmission rate of G. salaris between salmon placed floating in a larger fish tank (100 × 100 × 30 cm). The parr. Furthermore, in field studies we wanted to boxes were divided into two compartments by a polystyrene

Address for correspondence: A. Soleng, Zoological Museum, University of Oslo, Sars gate 1, N-0562 Oslo, Norway. Phone: ++47 2285 1762; Fax: ++47 2285 1837; E-mail: [email protected]

179 wall. The fish tank had a continuous flow of charcoal filtered RESULTS and dechlorinated laboratory fresh water (2 l/min), and an aquarium filter (Fluval 403 without filter medium; 1200 The effect of water temperature on the transmission l/hour) circulated the water. In the experiments at 1.2°C, rate of G. salaris – laboratory experiments however, there was no flow-through of the water, but it was There was a marked difference in the transmission recirculated through a cooler (Eheim type 3551). A trans- rate between the three tested temperatures, positively parent lid was placed over the boxes, while a semi-transparent correlated with temperature. At 1.2°C, 0.22% (range 0- lid was placed over the fish tanks to give a constant dim 0.78%) of the parasites on the donor fish successfully illumination. One experimentally infected salmon parr (donor transmitted to the recipient fish, at 4.7°C, 2.0% (range fish), with a known number of parasites, was placed in one 0-9.4%), while 4.9% (range 0-13.4%) transmitted at the compartment of a box together with one naive uninfected highest temperature of 12.2°C. The prevalence of salmon parr (recipient fish) for 24 hours. The number of infection on recipient fish after the exposure were 58.3, parasites on the donor fish varied considerably, at 1.2°C 87.9 and 95.2% at 1.2, 4.7 and 12.2°C, respectively. ranging from 243 to 536 (mean 394.5), at 4.7°C from 54 to Fig. 1 demonstrates the number of G. salaris on the 427 (mean 240.7), and at 12.2°C from 7 to 1100 (mean 302.0). recipient fish (after 24 hours exposure to the donor fish) After the exposure the number of parasites on the previously as a function of the initial number of G. salaris on the uninfected recipient fish was assessed. This procedure was repeated 12 times at 1.2°C, 33 times at 4.7°C and 83 times at donor fish at the three selected temperatures. 12.2°C. The fish were not fed during the experiments. Transmission of G. salaris to caged fish – field The number of parasites was assessed by counting the G. experiments salaris specimens on the external skin and fins of A total of 10 fish out of 157 fish (prevalence 6.4%) anaesthetised fish (cf. Bakke et al. 1991). Anaesthesia may be (three fish escaped during the collection) was found to stressful to the parasites, but Harris et al. (1994) reported that be infected with G. salaris after 24 hours in the cages. the mortality and fecundity schedules of G. salaris There were no difference in infection between experimentally derived by Jansen and Bakke (1991) are close longitudinally and transversally placed cages, so these to those occurring in natural infections, despite the data are pooled in Table 1. All 10 infected fish had one complications of frequent anaesthesia. The anaesthetic parasite each, and the sites of attachment were the solution used had the same temperature as in the respective experiments, and fresh solution was used for each fish. tailfin (in four cases), the pelvic fins (in two cases), the pectoral fins (in three cases) and the peduncle (in one Transmission of G. salaris to caged fish – field experiments case). No G. salaris was found in the oral cavity or on The experiments were performed in the end of August the gills. 1993 and beginning of July 1994. The water temperature in the river during the experiments was 12-14°C. Five individually separated small wire mesh cages (21 × 8 Table 1. Transmission of detached Gyrodactylus salaris × 7 cm) were placed hanging in tandem above the substrate drifting in the water column to Atlantic salmon (Salmo salar) inside a larger wire mesh cage (207 × 57 × 32 cm). Two such parr. The fish were individually isolated in mesh wire cages, large cages were placed on the river bottom, both longi- hanging above the substrate, inside larger mesh wire cages tudinally (8 replicates, totalling 80 fish) and transversally (8 placed in the River Lierelva (12-14°C) for 24 hours. replicates, totalling 80 fish) in relation to the water current, at a depth of approximately 60 cm. The water speed at the Time of Number Number of infected Mean surface was approximately 0.25 m/s. One uninfected naive experiments of fish fish (prevalence %) intensity salmon parr was placed inside each small mesh cage for 24 August 1993 80 4 (5.0) 1.0 hours, and thereafter fixed in 10% formaldehyde for later July 1994 77 (3 lost) 6 (7.8) 1.0 examinations for G. salaris. Only a negligible number of parasites detach during this fixation procedure (Appleby and Mo 1997; own observations). Table 2. Transmission of Gyrodactylus salaris to Atlantic salmon (Salmo salar) parr. Two-hundred marked adipose fin Transmission of G. salaris to fish released into the river – clipped fish were released into the River Lierelva (8°C) and field experiments caught by electro-fishing after 24 and 48 hours. Two-hundred uninfected salmon parr (marked by adipose fin clipping) were released in the river in the end of Time of Number of Mean September in 1993, in the same area as the cage experiments exposure in Number of infected fish intensity were performed. The water temperature in the river during the the river fish caught (prevalence %) (range) experiment was 8 °C. Twenty-four and 48 hours after the (hours) release the same river stretch was electro-fished, and all 24 18 8 (44.4) 1.9 (1-3) adipose fin clipped fish caught were fixed in 10% 48 19 11 (57.9) 2.3 (1-5) formaldehyde for later examinations for G. salaris.

180 Soleng et al.: Transmission of Gyrodactylus salaris

Transmission of G. salaris to fish released into the 4 river – field experiments A Eighteen of the 200 marked and released fish were caught after 24 hours and 19 after 48 hours. The 3 prevalence and mean intensity of infection increased

on recipient fish with the duration of the exposure (Table 2). Gyrodacty- 2 lus salaris specimens were found attached to all of the fins, the body and the head. No G. salaris was found in

G. salaris the oral cavity or on the gills. 1 DISCUSSION

Number of 0 The present results demonstrate the importance of 0 200 400 600 water temperature concerning the rate of transmission Number of G. salaris on donor fish of Gyrodactylus salaris. Increasing water temperature increases the rate of transmission as previously observed by Bakke et al. (1991) in the transmission of 40 G. salaris from salmon parr to resistant European eel. In B nature this phenomenon probably enhances G. salaris’ colonisation of the young of the year (0+) salmon parr as they emerge from the gravel in spring/summer during conditions of increasing temperature. The increased on recipient fish 20 parasite transmission at higher temperatures can probably be explained by increased parasite and/or host activity. In laboratory experiments Jansen and Bakke G. salaris (1991) demonstrated the importance of ambient water temperature for the population dynamics of G. salaris in fresh water. The survival time for individual parasites 0 Number of was negatively correlated with temperature, while the 0200400600mean number of offspring was optimal between 6.6 and Number of G. salaris on donor fish 13.0°C. The potential for population growth of G. salaris, however, was an increasing function of water temperatures, due to decreasing age of the parasites 80 when giving birth to consecutive offspring. Later C studies in nature (Jansen and Bakke 1993a,b, Appleby and Mo 1997) have supplemented these findings, 60 demonstrating seasonality in parasite abundance related to changing water temperatures. on recipient fish 40 One central enigma in the G. salaris-Atlantic salmon interaction is the transmission of G. salaris in relation to the reduction of the host population (Halvorsen and G. salaris 20 Hartvigsen 1989). Epidemiological theory, as well as laboratory and field experiments, suggest that when parasite transmission is direct, by host to host contact, Number of 0 the density of the host population must be above a 0 500 1000 1500 certain threshold for the parasites to persist or an Number of G. salaris on donor fish epidemic to occur in the host population (Anderson 1980, Anderson et al. 1981, Scott and Anderson 1984). In Norwegian salmon rivers, G. salaris is reported to be Fig. 1. Transmission rate of Gyrodactylus salaris between two highly pathogenic, reducing Atlantic salmon parr constrained Atlantic salmon (Salmo salar) parr in relation to density to close to zero during an epidemic (Heggberget ambient water temperature. The data points demonstrate the and Johnsen 1982, Johnsen and Jensen 1986, 1991). number of G. salaris on the recipient fish after 24 hours of exposure to the donor fish as a function of the initial Nevertheless, prevalences of 100% can still be observed number of G. salaris on the donor fish. (A) 1.2°C. (B) 4.7°C. in these declining host populations (Johnsen and Jensen (C) 12.2°C. The regression line for experiments at 12.2°C 1992). Salmon parr are territorial (Kalleberg 1958, is Y = -1.11 + 0,0529X (df. 1, 79; r2 = 0.52) where Y = Keenleyside 1962, Folmar and Dickhoff 1980), with recipient fish and X = donor fish. little direct contact (Keenleyside 1962). It is also known

181 that when populations are limited by processes other Platichthys flesus (L.), being infected with G. salaris in than competition, competition is of minimal intensity or a natural environment might also be an example of an non-existent (Hearn 1987), possibly reducing the indirect transmission from the substrate. Soleng and chance of direct contact between the salmon parr even Bakke (1998) found a higher transmission of G. salaris more. This implies that the importance of direct host to resistant flounder and nine-spined sticklebacks, contact for G. salaris transmission, accepted as the main Pungitius pungitius (L.) than to resistant three-spined route of dispersion among gyrodactylids (Bychowsky sticklebacks, Gasterosteus aculeatus L., in the 1957, Malmberg 1957, Bauer 1958, Scott and Anderson laboratory. They suggested that the difference could be 1984, Kamiso and Olson 1986), is questionable as caused by host behaviour, as the flounder and nine- suspected by Mo (1992). However, if other transmission spined stickleback had more direct contact with the routes are to alter the relationship between substratum than the three-spined stickleback. The pathogenicity and transmission they have to occur importance of dead infected hosts in the transmission of frequently. gyrodactylids is also noted (Scott and Anderson 1984, Bakke et al. (1992) suggested, that the role of Bakke et al. 1991, 1992). It is further known that drifting detached G. salaris in the water column may gyrodactylids tend to leave a dead host (Malmberg have been underestimated, as our present field results 1970, Harris 1980); over 50% of Gyrodactylus indicate. Furthermore, it is known that gyrodactylids gasterostei Gläser, 1974 had left the dead host after 18 may become detached from their hosts through hours at 15°C (Harris 1980). The activity of such accident, active migration or as a result of a host detached parasites seems also to increase (Harris 1980), response (Lester 1972, Scott and Anderson 1984), and possibly facilitating parasite transmission from the that higher temperatures lead to a higher degree of substrate. Transmission through predation has also been accidental dislodgement during transmission (Harris suggested as a possibility (Malmberg 1973, Harris and 1980). Scott and Anderson (1984) estimated a loss of Tinsley 1987, Mo 1987). 61-65% of Gyrodactylus turnbulli Harris, 1986 during Detached G. salaris drifting in the water column are transmission between guppies, Poecilia reticulata disseminated downstream watersheds, while mature Peters, at 25°C. Our present results, demonstrating that ascending adult salmon transport the parasite upstream, detached G. salaris in the planktonic drift have the even through fish ladders (Soleng et al. 1998). The potential to infect salmon parr at a relatively high rate, observed potential of transmission of detached parasites complement those of Parker (1965), who also reported to salmon parr in rivers might also be of importance the potential of detached gyrodactylids to attach to concerning a possible transmission of parasites to hosts fishes. The present study, however, also demonstrates a in brackish water. High numbers of detached G. salaris higher transmission rate of G. salaris to free-living parr are possibly drifting into estuaries from infected rivers compared to caged fish exposed only to drifting during peak epidemics. Soleng et al. (1998) reported detached parasites, even though the water temperature transmission of G. salaris in brackish water up to 20.0 was lower in the former case (8°C compared to 12- ‰ after direct host contact. Thus, drifting G. salaris 14°C). This emphasises the importance of other routes may infect hosts in estuaries, and still have a potential of transmission rather than through drift. Hoffman and for dispersal also to other rivers through brackish water Putz (1964) and Parker (1965) found a higher infection migration of infected hosts (Anonymous 1981, Johnsen level of gyrodactylids on fish which had access to the and Jensen 1986, Lund and Heggberget 1992, Soleng bottom compared to fish that were suspended in the and Bakke 1997, Soleng et al. 1998). water column. Indirect transmission from the substratum is likely to be especially important in the G. Acknowledgements. We thank the staff at DOFA (Drammen salaris-Atlantic salmon interaction, as salmon parr are og Omegn Fiskeadministrasjon) and Kjersti Kvalsvik at the bottom dwelling fish (Kalleberg 1958, Keenleyside Zoological Museum, University of Oslo, for technical 1962). Bakke et al. (1991) reported indirect assistance. Dr. Phil D. Harris, University of Nottingham, transmission of G. salaris from the substrate to kindly commented on the manuscript. This study was funded European eel, and the report of Mo (1987) of flounder, by the Norwegian Research Council.

REFERENCES ANDERSON R.M. 1980: Depression of host population ANONYMOUS 1981: Rapport fra Gyrodactylusutvalget over abundance by direct lifecycle macroparasites. J. Theor. virksomheten i 1980 og program for virksomheten i 1981. Biol. 82: 283-311. Direktoratet for naturforvaltning, Trondheim, 59 pp. ANDERSON R.M., JACKSON H.C., MAY R.H., SMITH APPLEBY C., MO T.A. 1997: Population dynamics of Gyro- A.D. 1981: Population dynamics of fox rabies in Europe. dactylus salaris (Monogenea) infecting Atlantic salmon, Nature 289: 765-771. Salmo salar, parr in the river Batnfjordselva, Norway. J. Parasitol. 83: 23-30.

182 Soleng et al.: Transmission of Gyrodactylus salaris

BAKKE T.A., HARRIS P.D., HANSEN L.P., JANSEN P.A. JOHNSEN B.O., JENSEN A.J. 1986: Infestations of Atlantic 1992: Host specificity and dispersal strategy in salmon, Salmo salar, by Gyrodactylus salaris in gyrodactylid monogeneans with particular reference to Norwegian rivers. J. Fish Biol. 26: 233-241. Gyrodactylus salaris (Platyhelminthes, Monogenea). Dis. JOHNSEN B.O., JENSEN A.J. 1991: The Gyrodactylus story Aquat. Org. 13: 45-57. in Norway. Aquaculture 98: 289-302. BAKKE T.A., JANSEN P.A., HANSEN L.P. 1991: JOHNSEN B.O., JENSEN A.J. 1992: Infection of Atlantic Experimental transmission of Gyrodactylus salaris salmon, Salmo salar L., by Gyrodactylus salaris, Malmberg, 1957 (Platyhelminthes, Monogenea) from the Malmberg 1957, in the River Lakselva, Misvær in Atlantic salmon (Salmo salar) to the European eel northern Norway. J. Fish Biol. 40: 433-444. (Anguilla anguilla). Can. J. Zool. 69: 733-737. KALLEBERG H. 1958: Observations in a stream tank of BAUER O.N. 1958: Parasitic diseases of cultured fishes and territoriality and competition in juvenile salmon and trout methods and their prevention and treatment. In: V.A. (Salmo salar L. and S. trutta L.). Rep. Inst. Freshwater Dogiel, G.K. Petrushevski, and Yu.I. Polyanski (Eds.), Res. Drottningholm 39: 55-98. Parasitology of Fishes. (Translated by Z. Kabata 1961.) KAMISO H.N., OLSON R.E. 1986: Host-parasite Oliver and Boyd Ltd, Edinburgh, pp. 267-300. relationships between Gyrodactylus stellatus (Monogenea: BYCHOWSKY B.E. 1957: Monogenetic Trematodes. Their Gyrodactylidae) and Parophrys vetulus (Pleuronectidae – Systematics and Phylogeny. Akad. Nauk USSR. (English English sole) from coastal waters of Oregon. J. Parasitol. translation by American Institute of Biological Sciences, 72: 125-129. Washington, D.C., 1961.) Graphic Arts Press, Inc., KEENLEYSIDE 1962: Skin-diving observations of Atlantic Washington, D.C., 1961, 627 pp. salmon and brook trout in the Miramichi River, New FOLMAR L.C., DICKHOFF W.W. 1980: The parr-smolt Brunswick. J. Fish. Res. Board Can. 19: 625-634. transformation and seawater adaptation in salmonids. LESTER R.J.G. 1972: Attachment of Gyrodactylus to Aquaculture 21: 1-37. Gasterosteus and host response. J. Parasitol. 58: 717-722. HALVORSEN O., HARTVIGSEN R. 1989: A review of the LUND R.A., HEGGBERGET T.G. 1992: Migration of biogeography and epidemiology of Gyrodactylus salaris. Atlantic salmon, Salmo salar L., parr through a NINA Utredning 2: 1-41. Norwegian fjord: potential infection path of Gyrodactylus HARRIS P.D. 1980: The behaviour of Gyrodactylus on living salaris. Aquac. Fish. Manage. 23: 367-372. hosts. Proceedings of the 3rd European Multicolloqium of MALMBERG G. 1957: Om förekomsten av Gyrodactylus på Parasitology, Cambridge 1980: 97. svenska fiskar. Skr. Söd. Sver. Fiskför. Årsskr. 1956: 19- HARRIS P.D., JANSEN P.A., BAKKE T.A. 1994: The 76. population age structure and reproductive biology of MALMBERG G. 1970: The excretory system and the Gyrodactylus salaris Malmberg (Monogenea). marginal hooks as a basis for the systematics of Parasitology 108: 167-173. Gyrodactylus (Trematoda, Monogenea). Ark. Zool. Ser. 2, HARRIS P.D., TINSLEY R.C. 1987: The biology of 23: 1-235. Gyrdicotylus gallieni (Gyrodactylidea), an unusual MALMBERG G. 1973: On a Gyrodactylus species from viviparous monogenean from the African clawed toad, Northern Sweden and the subgeneric position of G. hrabei Xenopus laevis. J. Zool. 212: 325-346. Ergens, 1957 (Trematoda, Monogenea). Zool. Scr. 2: 39- HEARN W.E. 1987: Interspecific competition and habitat 42. segregation among stream-dwelling trout and salmon: a MARGOLIS L., ESCH G.W., HOLMES J.C., KURIS A.M., review. Fisheries 12(5): 24-31. SCHAD G.A. 1982: The use of ecological terms in HEGGBERGET T.G., JOHNSEN B.O. 1982: Infestations by parasitology (report of an ad hoc committee of the Gyrodactylus sp. of Atlantic salmon, Salmo salar L., in American Society of Parasitologists). J. Parasitol. 68: 131- Norwegian rivers. J. Fish Biol. 21: 15-26. 133. HOFFMAN G.L., PUTZ R.E. 1964: Studies on Gyrodactylus MO T.A. 1987: Taxonomiske og biologiske undersøkelser. macrochiri n. sp. (Trematoda: Monogenea) from Lepomis Virksomheten i 1986 og forslag til virksomheten i 1987. macrochirus. Proc. Helminthol. Soc. Wash. 31: 76-82. Gyrodactylusundersøkelsene ved Zoologisk Museum, JANSEN P.A., BAKKE T.A. 1991: Temperature-dependent Universitetet i Oslo. Rapport nr. 2, 70 pp. reproduction and survival of Gyrodactylus salaris MO T.A. 1992: Seasonal variations in the prevalence and Malmberg, 1957 (Platyhelminthes: Monogenea) on infestation intensity of Gyrodactylus salaris Malmberg, Atlantic salmon (Salmo salar L.). Parasitology 102: 105- 1957 (Monogenea, Gyrodactylidae) on Atlantic salmon 112. parr, Salmo salar L., in the River Batnfjordselva, Norway. JANSEN P.A., BAKKE T.A. 1993a: Regulatory processes in J. Fish Biol. 41: 697-707. the monogenean Gyrodactylus salaris Malmberg-Atlantic PARKER J.D. 1965: Seasonal occurrence, transmission, and salmon (Salmo salar L.) association. I. Field studies in host specificity of the monogenetic trematode southeast Norway. Fish. Res. 17: 87-101. Gyrodactylus elegans from the golden shiner JANSEN P.A., BAKKE T.A. 1993b: Regulatory processes in (Notemigonus crysoleucas). Ph.D. thesis, Southern Illinois the monogenean Gyrodactylus salaris Malmberg-Atlantic University, 82 pp. salmon (Salmo salar L.) association. II. Experimental SCOTT M.E., ANDERSON R.M. 1984: The population studies. Fish. Res. 17: 103-114. dynamics of Gyrodactylus bullatarudis (Monogenea)

183 within laboratory populations of the fish host Poecilia (Platichthys flesus) to experimental infections with the reticulata. Parasitology 89: 159-194. monogenean Gyrodactylus salaris. Folia Parasitol. 45: SOLENG A., BAKKE T.A. 1997: Salinity tolerance of 270-274. Gyrodactylus salaris (Platyhelminthes, Monogenea): SOLENG A., BAKKE T.A., HANSEN L.P. 1998: Potential laboratory studies. Can. J. Fish. Aquat. Sci. 54: 1837- for dispersal of Gyrodactylus salaris (Platyhelminthes, 1845. Monogenea) by sea-running stages of the Atlantic salmon SOLENG A., BAKKE T.A. 1998: The susceptibility of three- (Salmo salar): field and laboratory studies. Can. J. Fish. spined stickleback (Gasterosteus aculeatus), nine-spined Aquat. Sci. 55: 507-514. stickleback (Pungitius pungitius) and flounder

Received 1 December 1998 Accepted 23 March 1999

184