Transmission of the Monogenean Gyrodactylus Salaris
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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.