Infestations of Atlantic salmon, Salmo salar, by Gyrodactylus salaris in Norwegian rivers

Over the 6 years 1980–85, 212 Norwegian rivers have been examined for occurrence of Gyrodactylus salaris: it was found in 26 rivers and six salmon hatcheries scattered throughout the country from Troms county in the north to Sogn og Fjordane in western Norway. The distribution of G. salaris is connected with the stocking of fish from infected salmon hatcheries. The populations of salmon parr have been drastically reduced in the infected rivers. In later years catches of ascending salmon in these rivers have also sharply declined: in 1984 salmon fishery losses were estimated at 250–500 t.
Gyrodactylus salaris is most probably a recent introduction to Norwegian rivers. A primary aim is to exterminate this parasite from all infected rivers and hatcheries: so far this has been accomplished in one river and one hatchery.     

High Gyrodactylus salaris infection rate in triploid Atlantic salmon Salmo salar

We describe an unusually high infection rate of Gyrodactylus salaris Malmberg in juvenile Atlantic salmon Salmo salar L. of Baltic Sea origin, which are generally believed to be more resistant to G. salaris than East Atlantic salmon populations. Based on analyses of mitochondrial (complete cytochrome oxidase 1 [CO1] gene, 1548 bp) and nuclear (ADNAM1, 435 bp; internal transcribed spacer [ITS] rDNA region, 1232 bp) DNA fragments, the closest relatives of the characterized Estonian G. salaris strain were parasites found off the Swedish west coast and in Raasakka hatchery, Iijoki (Baltic Sea, Finland). Analyses of 14 microsatellite loci of the host S. salarrevealed that approximately 40% of studied fish were triploids. We subsequently identified triploid Atlantic salmon of Baltic origin as more susceptible to G. salaris infection than their diploid counterparts, possibly due to compromised complement-dependent immune pathways in triploid salmon. This is in accordance with earlier studies that have shown elevated susceptibility of triploids to various viral or bacterial pathogens, and represents one of the first reports of increased susceptibility of triploid salmonid fish to an ectoparasite. However, further experimental work is needed to determine whether triploid Atlantic salmon is generally more susceptible to G. salaris compared to their diploid counterparts, irrespective of the particular triploidization method and population of origin.     

Geographic risk factors for inter-river dispersal of Gyrodactylus salaris in fjord systems in Norway

Gyrodactylus salaris has been recorded in 46 Norwegian rivers since 1975 and is considered a threat to Atlantic salmon stocks. The primary introductions of G. salaris (primary infected rivers) have been accounted for by specific events, as reported in the literature. The parasite has subsequently dispersed to adjacent localities (secondary infected rivers). The objective of this paper is to address the occurrence of secondary infections by examining the hypothesis of inter-river dispersal of G. salaris. A dispersal model for the secondary river infections via migrating infected fish is proposed. Due to the limited tolerance of G. salaris to salinity, both freshwater inflow to dispersal pathways and dispersal distance were expected to influence the probability of inter-river dispersal. Eighteen rivers were categorised as primary infected rivers, 28 as secondary infected rivers, and 54 as rivers at risk. Four risk factors: the log10 freshwater inflow; the dispersal distance; the time at risk; and the salmon harvest were combined in a multi-variable logistic regression model of the probability of secondary infection. The final multi-variable model included log10 freshwater inflow (Wald chi-square = 9.93) and dispersal distance (Wald chi-square = 6.48). Receiver operating characteristic analyses of the final model supported freshwater inflow as a strong predictor of G. salaris infection status. The strong influence of the freshwater inflow on the probability of secondary infection adds further support to the hypothesis of inter-river dispersal of G. salaris through fjords.     

The ultrastructure of hypersymbionts on the monogenean Gyrodactylus salaris infecting Atlantic salmon Salmo salar

There is increasing pressure to develop alternative control strategies against the pathogen Gyrodactylus salaris, which has devastated wild Atlantic salmon Salmo salar in Norway. Hyperparasitism is one option for biological control and electron microscopy has revealed two ectosymbionts associated with G. salaris: unidentified rod-shaped bacteria, and the protist, Ichthyobodo necator. No endosymbionts were detected. The flagellate I. necator occurred only occasionally on fish suffering costiosis, whereas bacterial infections on the tegument of G. salaris were observed throughout the year, but at variable densities. Bacteria were seldom observed attached to fish epidermis, even when individuals of G. salaris on the same host were heavily infected. Wounds on salmon epidermis caused by the feeding activity of bacteria-infected G. salaris did not appear to be infected with bacteria. On heavily infected gyrodactylids, bacteria were most abundant anteriorly on the cephalic lobes, including the sensory structures, but no damaged tissue was detected by transmission electron microscopy in the region of bacterial adherence. Furthermore, transmission and survival of infected G. salaris on wild salmon did not appear to be influenced by the bacterial infection. The lack of structural damage and impact on G. salaris biology indicates that these bacteria are not a potential agent for control of gyrodactylosis. However, this may not be the case for all gyrodactylid-bacterial interactions and a review of bacterial infections of platyhelminths is presented.     

Identification of genetic markers associated with Gyrodactylus salaris resistance in Atlantic salmon Salmo salar

Gyrodactylus salaris Malmberg, 1957 is a freshwater monogenean ectoparasite of salmonids, first recorded in Norway in 1975 and responsible for extensive epizootics in wild Atlantic salmon Salmo salar L. The susceptibility of different populations of Atlantic salmon to G. salaris infection differs markedly, with fish from the Baltic being characterised as relatively resistant whereas those from Norway or Scotland are known to be (extremely) susceptible. Resistance to Gyrodactylus infection in salmonids has been found to be heritable and a polygenic mechanism of control has been hypothesised. The current study utilises a 'Quantitative trait loci' (QTL) screening approach in order to identify molecular markers linked to QTL influencing G. salaris resistance in B1 backcrosses of Baltic and Scottish salmon. Infection patterns in these fish exhibited 3 distinct types; susceptible (exponential parasite growth), responding (parasite load builds before dropping) and resistant (parasite load never increases). B1 backcross fish were screened at 39 microsatellite markers and single marker-trait associations were examined using general linear modelling. We identified 10 genomic regions associated with heterogeneity in both innate and acquired resistance, explaining up to 27.3% of the total variation in parasite loads. We found that both innate and acquired parasite resistance in Atlantic salmon are under polygenic control, and that salmon would be well suited to a selection programme designed to quickly increase resistance to G. salaris in wild or farmed stocks.     

A Monte Carlo simulation model for assessing the risk of introduction of Gyrodactylus salaris to the Tana river, Norway.

The Tana river in northern Norway, the most productive salmon river in Europe, is free of Gyrodactylus salaris. Currently there is one salmon farm in operation on the Tana fjord. Because of the strong association between stocking of rivers with salmon and infestations with G. salaris there is national and international concern that the existing farm might lead to the introduction of the parasite to the Tana river. In response to these concerns a quantitative analysis of the risk of introduction of G. salaris to the Tana river was undertaken. A scenario tree, the Monte Carlo simulation model and results of the simulations including sensitivity analyses are presented and discussed. Results show that the probability of introduction of G. salaris to the Tana river via transfer of smolt to the existing salmon farm is extremely low primarily due to the low probability that the transferred smolt become infested. The total risk was very sensitive to changes in the salinity of the water at the sea site.     

Evidence for episodic acidification effects on migrating Atlantic salmon Salmo salar smolts

Field studies were conducted to determine levels of gill aluminium as an index of acidification effects on migrating Atlantic salmon Salmo salar smolts in the north‐eastern U.S.A. along mainstem river migration corridors in several major river basins. Smolts emigrating from the Connecticut River, where most (but not all) tributaries were well buffered, had low or undetectable levels of gill aluminium and high gill Na⁺/K⁺‐ATPase (NKA) activity. In contrast, smolts emigrating from the upper Merrimack River basin where most tributaries are characterized by low pH and high inorganic aluminium had consistently elevated gill aluminium and lower gill NKA activity, which may explain the low adult return rates of S. salar stocked into the upper Merrimack catchment. In the Sheepscot, Narraguagus and Penobscot Rivers in Maine, river and year‐specific effects on gill aluminium were detected that appeared to be driven by underlying geology and high spring discharge. The results indicate that episodic acidification is affecting S. salar smolts in poorly buffered streams in New England and may help explain variation in S. salar survival and abundance among rivers and among years, with implications for the conservation and recovery of S. salar in the north‐eastern U.S.A. These results suggest that the physiological condition of outmigrating smolts may serve as a large‐scale sentinel of landscape‐level recovery of atmospheric pollution in this and other parts of the North Atlantic region.     

Susceptibility of Baltic and East Atlantic salmon Salmo salar stocks to Gyrodactylus salaris (Monogenea)

The susceptibility of a Baltic salmon stock Salmo salar (Indals?lv, central Sweden) to Norwegian Gyrodactylus salaris (Figga strain, central Norway) was experimentally tested and compared with previously obtained results on East Atlantic salmon (Lierelva, SE Norway). Contrary to expectation, the Baltic salmon, which had no prior exposure to this parasite strain, appeared almost as susceptible as the Norwegian salmon parr that naturally experience G. salaris-induced mortality. Individually isolated salmon of both stocks sustained G. salaris infections with little evidence of innate resistance. A few individuals of the Indals?lv stock controlled their infection from the beginning, but overall there was considerable heterogeneity in the course of infection in both stocks. On individual hosts, G. salaris growth rates declined steadily throughout the infection, a trend which was particularly marked amongst the Lierelva stock. On shoaling Lierelva fish, there was some evidence of reduced parasite population growth towards the end of the infection; this was not apparent in Indals?lv fishes. These results reflect a growing awareness that not all Baltic salmon may be resistant to Norwegian G. salaris, and that Norwegian and Baltic G. salaris strains may differ in virulence. Consequently, management decisions concerning this parasite-host system should be based upon the actual, and tested, susceptibility of stocks under consideration and not upon identification of stocks as either Atlantic or Baltic.     

Infection of Atlantic salmon, Salmo salar L., by Gyrodactylus salaris, Malmberg 1957, in the River Lakselva, Misvær in northern Norway

Gyrodacrylus salaris was most probably introduced to the River Lakselva in 1975 through stocking of Atlantic salmon from an infected hatchery. The parasite population grew rapidly, and the parasite spread throughout the entire watercourse during the summer of 1976. This epidemic situation led to mortality among the young Atlantic salmon, and the density of salmon parr was heavily reduced from 1976 to 1977. The density of salmon parr has remained close to zero since then, while there are no apparent trends toward decrease or increase in the density of brown trout. In spite of the reduced density of young salmon, a new epidemic has developed each year among the few young 0+ and 1+ Atlantic salmon present in the river. Results from successive sampling during the summer of 1987, 1988 and 1989 indicate that most of the presmolt salmon are attacked during their first summer or autumn of life. The infection develops into an epidemic during the first autumn, winter or the next summer. The build-up of the parasite burden on the fish leads in turn to mortality. Norwegian Atlantic salmon probably have no resistance against G. salaris, since the parasite has recently been introduced to Norwegian rivers.     

Survival of migrating salmon smolts in large rivers with and without dams

The mortality of salmon smolts during their migration out of freshwater and into the ocean has been difficult to measure. In the Columbia River, which has an extensive network of hydroelectric dams, the decline in abundance of adult salmon returning from the ocean since the late 1970s has been ascribed in large measure to the presence of the dams, although the completion of the hydropower system occurred at the same time as large-scale shifts in ocean climate, as measured by climate indices such as the Pacific Decadal Oscillation. We measured the survival of salmon smolts during their migration to sea using elements of the large-scale acoustic telemetry system, the Pacific Ocean Shelf Tracking (POST) array. Survival measurements using acoustic tags were comparable to those obtained independently using the Passive Integrated Transponder (PIT) tag system, which is operational at Columbia and Snake River dams. Because the technology underlying the POST array works in both freshwater and the ocean, it is therefore possible to extend the measurement of survival to large rivers lacking dams, such as the Fraser, and to also extend the measurement of survival to the lower Columbia River and estuary, where there are no dams. Of particular note, survival during the downstream migration of at least some endangered Columbia and Snake River Chinook and steelhead stocks appears to be as high or higher than that of the same species migrating out of the Fraser River in Canada, which lacks dams. Equally surprising, smolt survival during migration through the hydrosystem, when scaled by either the time or distance migrated, is higher than in the lower Columbia River and estuary where dams are absent. Our results raise important questions regarding the factors that are preventing the recovery of salmon stocks in the Columbia and the future health of stocks in the Fraser River.     

Cloning,purification, kinetic and anion inhibition studies of a recombinant β-carbonic anhydrase from the Atlantic salmon parasite platyhelminth Gyrodactylus salaris

A β-class carbonic anhydrase (CA, EC 4.2.1.1) was cloned from the genome of the Monogenean platyhelminth Gyrodactylus salaris, a parasite of Atlantic salmon. The new enzyme, GsaCAβ has a significant catalytic activity for the physiological reaction, CO₂ + H₂O ⇋ HCO₃⁻ + H⁺ with a k_cat of 1.1 × 10⁵ s⁻¹ and a k_cat/K_m of 7.58 × 10⁶ M⁻¹ × s⁻¹. This activity was inhibited by acetazolamide (K_I of 0.46 µM), a sulphonamide in clinical use, as well as by selected inorganic anions and small molecules. Most tested anions inhibited GsaCAβ at millimolar concentrations, but sulfamide (K_I of 81 µM), N,N-diethyldithiocarbamate (K_I of 67 µM) and sulphamic acid (K_I of 6.2 µM) showed a rather efficient inhibitory action. There are currently very few non-toxic agents effective in combating this parasite. GsaCAβ is subsequently proposed as a new drug target for which effective inhibitors can be designed.     

Counterintuitive migration patterns by Atlantic salmon Salmo salar smolts in a large lake

What little is known about the seaward migration of Salmo salar smolt migration through standing waters indicates that it is both slow and results in high mortality rates, compared with riverine migration. This may be partly because smolts in lakes need to swim more actively and require more complex directional cues than they do in rivers. In this telemetry study of smolt migration through Loch Lomond, S. salar smolts made repeated movements in directions away from the outflowing river, which considerably increased migration time.     

Infestations by Gyrodactylus sp. of Atlantic salmon, Salmo salar L., in Norwegian rivers

Young Atlantic salmon, Salmo salar , brown trout, Salmo trutta , and Arctic char, Salvelinus alpinus , from eight rivers in North and Mid Norway were examined for Gyrodactylus. The fish were collected from 1975 to 1980. A Gyrodactylus salaris type was observed infecting salmon from six of these rivers. No trout or char were infected. A high frequency and intensity of infection of salmon were observed in all but one of the rivers surveyed. In the Saltdalselva, only one specimen of Gyrodactylus infecting one fish was observed. No subsequent mortality of salmon was observed in this river while there were signs of a high mortality of salmon in the other rivers. The salmon parr were more frequently attacked than the fry, the mortality of salmon seemed to have happened in most of the rivers one year after the first observations of Gyrodactylus were made. The mortality of salmon and the high infection rate of Gyrodactylus in these rivers appears unique, and as far as known to the authors there are no other described cases of mortality due to Gyodactylus in Atlantic salmon in natural waters. The reasons for the outbreak of Gyrodactylus in these rivers are not known. Two theories are discussed: one that the fish were weakened by environmental factors and the other that Gyrodactylus was introduced from some of the infected salmon hatcheries in Scandinavia.     

Isolation of a novel fish thymidylate kinase gene, upregulated in Atlantic salmon (Salmo salar L.) following infection with the monogenean parasite Gyrodactylus salaris

Analysis of differential gene expression in salmon (Salmo salar) blood following infection with the monogenean parasite Gyrodactylus salaris, resulted in the isolation of a thymidylate kinase gene not previously described from fish and which showed similarity to an LPS-inducible thymidylate kinase gene isolated from mouse macrophages. This salmon TYKi-like gene may play a role in an innate generalised response to pathogen infection as it was upregulated in salmon following infection with the parasite, and also in response to injection with the immunostimulants LPS and Poly I:C, used to emulate bacterial and viral infections, respectively. The possible role of this gene in the biosynthesis of mitochondrial DNA in activated macrophages, in response to G. salaris infection is discussed.     

Tracking Atlantic salmon smolts, Salmo salar L., through Loch Voil, Scotland

Twenty-two salmon smolts, Salmo salar L., carrying miniature sonic tags were tracked individually for periods of up to 175 h in Loch Voil, Scotland, during May 1979 and 1980. Activity was predominantly nocturnal, 80% occurring between 21.00 and 06.00 hours, and was apparently undirected. Average velocities during this active interval were 0.6 body lengths per second (bl s⁻¹), with 98 and 93% of the time spent moving at less than 2 and less than 1 bl s⁻¹, respectively. The rates of downstream displacement were 0.04 bl s⁻¹ in 1979 and 0.01 bl s⁻¹ in 1980. The direction of displacement of smolts and of movement of water at a depth of 1 m was positively correlated ( P <0.001) and smolt displacement was biassed slightly ahead of water movement. Mean step lengths were 141 and 200 m in 1979 and 1980, respectively. Rates of downstream passage of 327 ICES plate-tagged smolts released 16.8 km upstream of the fish trap at Clunie dam, Loch Tummel, during the spring migrations of 1975 and 1976 averaged 0.13 bl s⁻¹ in each year: net surface water movement was about 3.7 times this rate during the same intervals. These data are consistent with the model of passive smolt migration postulated by Tytler et al. (1978) and suggest that the active component required to ensure passage through a loch (Thorpe & Morgan, 1978) is very small.     

Estuarine survival and migratory behaviour of Atlantic salmon Salmo salar smolts

To estimate mortality rates, assess the spatio‐temporal dynamics of natural mortality and examine migratory behaviour during the fresh to saltwater transition, 185 wild Atlantic salmon Salmo salar smolts were implanted with coded acoustic transmitters. Seaward migration of tagged S. salar from four river systems in an area of Nova Scotia, Canada known as the Southern Upland was monitored using fixed receivers and active telemetry over 3 years. Cumulative survival through the river, inner estuary, outer estuary and bay habitats averaged 59·6% (range = 39·4–73·5%). When standardized to distance travelled, survival rates followed two patterns: (1) constant rates of survival independent of habitat or (2) low survival most frequently associated with inner estuary habitats. In rivers where survival was independent of habitat, residency periods were also independent of habitat, post‐smolts exhibited few upstream movements, took a more direct route to the ocean and reached the ocean rapidly. Alternatively, in rivers where survival was habitat specific, residency was also habitat specific with overall increased residency, more frequent upstream movements and delayed arrival to the open ocean. The sudden disappearance of most (75–100%) smolts and post‐smolts assumed dead during the course of this study warrants further examination into the role of avian predators as a mortality vector.     

Body and scale growth of wild Atlantic salmon smolts during seaward emigration

The relationship between scale and body growth for emigrating Atlantic salmon, Salmo salar, smolts was previously not understood and therefore was examined in this study using mark-recapture techniques. The size of smolts at time of recapture was significantly greater than when marked (P = 0.0002). The growth in length of smolts emigrating 5 km over an average of 20 days was 7.7 ± 6.1 mm per day. Instantaneous somatic growth (G _body) ranged from 7.0 × 10⁻⁴ to 5.1 × 10⁻³ (mean = 2.7 × 10⁻³ ± 1.3 × 10⁻³). The mean number of plus growth circuli present per scale was significantly greater for smolts when recaptured compared to when marked (P = 0.0014). The instantaneous growth rate of scales (G _scale) ranged from 1.4 × 10⁻³ to 11.5 × 10⁻³ (mean = 6.6 × 10⁻³ ± 4.3 × 10⁻³). The relationship between body size and scale radius showed positive allometry rather than isometry. The relationship of G _scale with G _body showed positive allometry indicating that scales grew at a slightly faster rate than the body during the emigratory period.     

Genetic differences in physiology, growth hormone levels and migratory behaviour of Atlantic salmon smolts

Out of five strains of Atlantic salmon Salmo salar of 1+ years released upstream of a fyke net in the River Gudenaa in 1996, three, Lagan, Ätran and Corrib, migrated immediately, 50% of the recaptured fish reaching the net in 3–6 days. Burrishoole and Conon fish migrated with a 15–19 day delay. Smolt development in 1997 at the hatchery showed a spring surge in gill Na⁺, K⁺-ATPase activity in all strains which was correlated with increased seawater tolerance. Differences in the timing of gill enzyme development matched the observed migration pattern well. Lagan, Ätran and Corrib strains reached high enzyme activity earlier than the Burrishoole and Conon strains, and strains with delayed enzyme development and migration showed a delayed regression of seawater tolerance compared with the early strains. Inter-strain differences in plasma growth hormone profiles could not be related to the observed patterns of Na⁺, K⁺-ATPase and seawater tolerance development. The study gives evidence of genetic influence on the timing and intensity of smolting and subsequent migration in Atlantic salmon.     

Seasonal dynamic of the infestation of young landlocked salmon (Salmo salar morpha sebago, Girard) by the monogenean species Gyrodactylus salaris

Seasonal dymanic of the infestation of young landlocked salmon (Salmo salar morpha sebago, Girard) by the monogenean species Gyrodactylus salaris Malberg, 1957 was studied in the river Lizhma, Karelia. It is established, that the temperature optimal for the development and reproduction of the parasite is about 3-8 degrees C. It is stated, that the abundance of G. salaris in the river Lizhma do not reach so high values, as it was observed in the regions outside the natural area of the parasite.