Sea lice and salmon population dynamics: effects of exposure time for migratory fish

The ecological impact of parasite transmission from fish farms is probably mediated by the migration of wild fishes, which determines the period of exposure to parasites. For Pacific salmon and the parasitic sea louse, Lepeophtheirus salmonis, analysis of the exposure period may resolve conflicting observations of epizootic mortality in field studies and parasite rejection in experiments. This is because exposure periods can differ by 2–3 orders of magnitude, ranging from months in the field to hours in experiments. We developed a mathematical model of salmon–louse population dynamics, parametrized by a study that monitored naturally infected juvenile salmon held in ocean enclosures. Analysis of replicated trials indicates that lice suffer high mortality, particularly during pre-adult stages. The model suggests louse populations rapidly decline following brief exposure of juvenile salmon, similar to laboratory study designs and data. However, when the exposure period lasts for several weeks, as occurs when juvenile salmon migrate past salmon farms, the model predicts that lice accumulate to abundances that can elevate salmon mortality and depress salmon populations. The duration of parasite exposure is probably critical to salmon–louse population dynamics, and should therefore be accommodated in coastal planning and management where fish farms are situated on wild fish migration routes.     

The Interaction between Water Currents and Salmon Swimming Behaviour in Sea Cages

Positioning of sea cages at sites with high water current velocities expose the fish to a largely unknown environmental challenge. In this study we observed the swimming behaviour of Atlantic salmon (Salmo salar L.) at a commercial farm with tidal currents altering between low, moderate and high velocities. At high current velocities the salmon switched from the traditional circular polarized group structure, seen at low and moderate current velocities, to a group structure where all fish kept stations at fixed positions swimming against the current. This type of group behaviour has not been described in sea cages previously. The structural changes could be explained by a preferred swimming speed of salmon spatially restricted in a cage in combination with a behavioural plasticity of the fish.     

Modeling Parasite Dynamics on Farmed Salmon for Precautionary Conservation Management of Wild Salmon

Conservation management of wild fish may include fish health management in sympatric populations of domesticated fish in aquaculture. We developed a mathematical model for the population dynamics of parasitic sea lice (Lepeophtheirus salmonis) on domesticated populations of Atlantic salmon (Salmo salar) in the Broughton Archipelago region of British Columbia. The model was fit to a seven-year dataset of monthly sea louse counts on farms in the area to estimate population growth rates in relation to abiotic factors (temperature and salinity), local host density (measured as cohort surface area), and the use of a parasiticide, emamectin benzoate, on farms. We then used the model to evaluate management scenarios in relation to policy guidelines that seek to keep motile louse abundance below an average three per farmed salmon during the March–June juvenile wild Pacific salmon (Oncorhynchus spp.) migration. Abiotic factors mediated the duration of effectiveness of parasiticide treatments, and results suggest treatment of farmed salmon conducted in January or early February minimized average louse abundance per farmed salmon during the juvenile wild salmon migration. Adapting the management of parasites on farmed salmon according to migrations of wild salmon may therefore provide a precautionary approach to conserving wild salmon populations in salmon farming regions.     

Using Agent-Based Modelling to Predict the Role of Wild Refugia in the Evolution of Resistance of Sea Lice to Chemotherapeutants

A major challenge for Atlantic salmon farming in the northern hemisphere is infestation by the sea louse parasite Lepeophtheirus salmonis. The most frequent method of controlling these sea louse infestations is through the use of chemical treatments. However, most major salmon farming areas have observed resistance to common chemotherapeutants. In terrestrial environments, many strategies employed to manage the evolution of resistance involve the use of refugia, where a portion of the population is left untreated to maintain susceptibility. While refugia have not been deliberately used in Atlantic salmon farming, wild salmon populations that migrate close to salmon farms may act as natural refugia. In this paper we describe an agent-based model that explores the influence of different sizes of wild salmon populations on resistance evolution in sea lice on a salmon farm. Using the model, we demonstrate that wild salmon populations can act as refugia that limit the evolution of resistance in the sea louse populations. Additionally, we demonstrate that an increase in the size of the population of wild salmon results in an increased effect in slowing the evolution of resistance. We explore the effect of a population fitness cost associated with resistance, finding that in some cases it substantially reduces the speed of evolution to chemical treatments.     

A model of salmon louse production in Norway: effects of increasing salmon production and public management measures.

Salmon lice Lepeophtheirus salmonis Kr?yer have caused disease problems in farmed Atlantic salmon Salmo salar L. since the mid-1970s in Norway. High infection intensities and premature return of wild sea trout Salmo trutta L. were first reported in 1992. Later emaciated wild Atlantic salmon smolts carrying large amounts of lice have been observed both in fjords and offshore. The Norwegian Animal Health Authority regulations to control the problem, which came into operation in 1998, included compulsory louse level monitoring in farms and maximum legal numbers of lice per fish. Here, we present a model of salmon louse egg production in Norway and show that the effect of the current public management strategy is critically dependent on the yearly increase in salmon production. This is because the infection pressure is the product of the number of fish in the system, and the number of lice per fish. Due to the much larger number of farmed than wild salmonids, it is highly likely that lice originating from farmed salmon infect wild stock. Estimated tolerance limits for wild salmonids vary widely, and the level of louse egg production in farms which would be needed to decimate wild populations is not known. Two possible thresholds for total lice egg production are investigated: (1) 1986 to 1987 level (i.e. before adverse effects on sea trout were recorded), and (2) a level corresponding to a doubling of the estimated natural infection pressure. The farm lice per fish limits that would have to be observed to keep louse production within the 2 thresholds are calculated for the period 1986 to 2005. A steady decrease in the permitted number of lice per fish may keep the total louse production stable, but the number of salmon required for verification of lice numbers will increase as the prevalence to be verified is decreased. At threshold (2), the model estimated that lice limits should have been 0.05 louse per fish in 1999. This would require 60 fish from each pen to be collected, anaesthetised and examined for a good estimate at a confidence level of 95%. Such sample numbers are likely to be opposed by farmers. The use of national delousing programs to solve the problem is discussed.     

Evaluating the effect of clustering when monitoring the abundance of sea lice populations on farmed Atlantic salmon

Using cluster random sampling theory and empirical estimates of the intra‐class correlations for sea lice Lepeophtheirus salmonis abundances, methods on how best to sample Atlantic salmon Salmo salar from cages on farms were derived. Estimates of intra‐class correlations for the abundance of the chalimus and mobile sea lice stages on Atlantic salmon in Scottish farms are given. These correlations were higher for mobile stages than for chalimus, and they had a substantive effect on increasing the number of cages and fish to be sampled for all sea lice stages. An important finding is that it is better to have a procedure that randomly samples a large number of cages using a small number of fish from each. This finding and the cluster random sampling approach have relevance to the monitoring of all marine species being farmed in cages or tanks.     

Intestinal barrier function of Atlantic salmon (<Emphasis Type="Italic">Salmo salar</Emphasis> L.) post smolts is reduced by common sea cage environments and suggested as a possible physiological welfare indicator

Background  

Fish farmed under high intensity aquaculture conditions are subjected to unnatural environments that may cause stress. Therefore awareness of how to maintain good health and welfare of farmed fish is important. For Atlantic salmon held in sea cages, water flow, dissolved oxygen (DO) levels and temperature will fluctuate over time and the fish can at times be exposed to detrimentally low DO levels and high temperatures. This experimental study investigates primary and secondary stress responses of Atlantic salmon post smolts to long-term exposure to reduced and fluctuating DO levels and high water temperatures, mimicking situations in the sea cages. Plasma cortisol levels and cortisol release to the water were assessed as indicators of the primary stress response and intestinal barrier integrity and physiological functions as indicators of secondary responses to changes in environmental conditions.     

Randomized clinical trial to investigate the effectiveness of teflubenzuron for treating sea lice on Atlantic salmon

A double-blind, randomized control clinical trial was performed to investigate the effectiveness of teflubenzuron in controlling sea lice Lepeophtheirus salmonis on farmed Atlantic salmon Salmo salar. A total of 40 sea cages from 3 commercial cage sites in Atlantic Canada were used in this Good Clinical Practice (GCP) trial. The teflubenzuron was administered in the feed at a dosage of 10 mg kg(-1) biomass d(-1) for 7 d. Medicated and control cages were matched by site, cage size, and pre-treatment mean lice counts using cages as the unit of concern. Post-treatment lice counts and staging of developmental stages were performed at 1 and 2 wk after the end of treatment. Chalimus stages in medicated cages were significantly lower than in control cages at 1 wk (79% reduction in mean lice counts, p < 0.001), and at 2 wk (53% reduction, p < 0.001). Mobile (pre-adult and adult) stages were also significantly reduced in medicated cages at 1 wk (69% reduction, p < 0.01), and at 2 wk (40% reduction, p < 0.01) post-treatment, respectively. Teflubenzuron was proven effective for reducing lice burdens on salmon despite the low parasite levels experienced during the trial and the recruitment of lice from the untreated cages. The use of cage as the unit of concern was an important design component of this trial.     

Identifying ‘firebreaks’ to fragment dispersal networks of a marine parasite

Marine ecosystems are beset by disease outbreaks, and efficient strategies to control dispersal of pathogens are scarce. We tested whether introducing no-farming areas or ‘firebreaks’ could disconnect dispersal networks of a parasitic disease affecting the world’s largest marine fish farming industry (～1000 farms). Larval salmon lice (Lepeophtheirus salmonis) are released from and transported among salmon farms by ocean currents, creating inter-farm networks of louse dispersal. We used a state-of-the-art biophysical model to predict louse movement along the Norwegian coastline and network analysis to identify firebreaks to dispersal. At least one firebreak that fragmented the network into two large unconnected groups of farms was identified for all seasons. During spring, when wild salmon migrate out into the ocean, and louse levels per fish at farms must be minimised, two effective firebreaks were created by removing 13 and 21 farms (1.3% and 2.2% of all farms in the system) at ～61°N and 67°N, respectively. We have demonstrated that dispersal models coupled with network analysis can identify no-farming zones that fragment dispersal networks. Reduced dispersal pathways should lower infection pressure at farms, slow the evolution of resistance to parasite control measures, and alleviate infection pressure on wild salmon populations.     

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.     

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.     

Qualitative analysis of the risk of introducing Gyrodactylus salaris into the United Kingdom

Gyrodactylus salaris is a freshwater, monogenean ectoparasite of Baltic strains of Atlantic salmon Salmo salar on which it generally causes no clinical disease. Infection of other strains of Atlantic salmon in Norway has resulted in high levels of juvenile salmon mortality and highly significant reductions in the population. The parasite is a major exotic disease threat to wild Atlantic salmon in the UK. This paper qualitatively assesses the risk of introduction and establishment of G. salaris into the UK. The current UK fish health regime prevents the importation of live salmonids from freshwater in territories that have not substantiated freedom from G. salaris. The importation of other species, e.g. eels Anguilla anguilla and non-salmonid fish, represents a low risk because the likelihood of infection is very low and the parasite can only survive on these hosts for less than 50 d. Importation of salmon carcasses presents a negligible risk because harvested fish originate from seawater sites and the parasite cannot survive full strength salinity. The importation of rainbow trout Oncorhynchus mykiss carcasses from G. salaris infected freshwater sites might introduce the parasite, but establishment is only likely if carcasses are processed on a salmonid farm in the UK. A number of mechanical transmission routes were considered (e.g. angling equipment, canoes, ballast water) and the most important was judged to be the movement of live fish transporters from farms on mainland Europe direct to UK fish farms. In the future, territories may have to substantiate freedom from G. salaris and economic drivers for live salmonid imports may strengthen. Under these circumstances, legal or illegal live salmonid imports would become the most significant risk of introduction.     

Vector potential of the salmon louse Lepeophtheirus salmonis in the transmission of infectious haematopoietic necrosis virus (IHNV)

To better understand the role of vector transmission of aquatic viruses, we established an in vivo virus-parasite challenge specifically to address (1) whether Lepeophtheirus salmonis can acquire infectious haematopoietic necrosis virus (IHNV) after water bath exposure or via parasitizing infected Atlantic salmon Salmo salar and if so, define the duration of this association and (2) whether L. salmonis can transmit IHNV to naive Atlantic salmon and whether this transmission requires attachment to the host. Salmon lice which were water bath-exposed to 1 x 10(5) plaque-forming units (pfu) ml(-1) of IHNV for 1 h acquired the virus (2.1 x 10(4) pfu g(-1)) and remained IHNV-positive for 24 h post exposure. After parasitizing IHNV-infected hosts (viral titer in fish mucus 3.3 x 10(4) pfu ml(-1)) salmon lice acquired IHNV (3.4 x 10(3) pfu g(-1)) and remained virus-positive for 12 h. IHNV-positive salmon lice generated through water bath exposure or after parasitizing infected Atlantic salmon successfully transmitted IHNV, resulting in 76.5 and 86.6% of the exposed Atlantic salmon testing positive for IHNV, respectively. In a second experiment, only salmon lice that became IHNV-positive through water bath exposure transmitted IHNV to 20% of the naive fish, and no virus was transmitted when IHNV-infected salmon lice were cohabitated but restrained from attaching to naive fish. Under laboratory conditions, adult L. salmonis can acquire IHNV and transmit it to naive Atlantic salmon through parasitism. However, the ephemeral association of IHNV with L. salmonis indicates that the salmon louse act as a mechanical rather than a biological vector or reservoir.     

Changes in hydrolytic enzyme activities of naïve Atlantic salmon Salmo salar skin mucus due to infection with the salmon louse Lepeophtheirus salmonis and cortisol implantation

The changes in the activities of mucus hydrolytic enzymes and plasma cortisol levels were examined following infection of Atlantic salmon Salmo salar with the salmon louse Lepeophtheirus salmonis and these changes were compared with those resulting from elevated plasma cortisol. Salmon were infected at high (Trial 1; 178 +/- 67) and low (Trial 2; 20 +/- 13) numbers of lice per fish and the activities of proteases, alkaline phosphatase, esterase and lysozyme in the mucus, as well as plasma cortisol levels were determined. At both levels of infection, there were significant increases of protease activity over time (1-way K-WANOVA; Trial 1, p = 0.004; Trial 2, p < 0.001). On several sampling days, generally on later days in the infections, the mucus protease activities of infected fish were significantly higher than control fish (Student's t-tests; p < 0.05). In addition, zymography experiments demonstrated bands of proteases at 17 to 22 kDa in the mucus of infected salmon that were absent in the mucus from non-infected fish and absent in the plasma of salmon. The intensity of these protease bands increased in the mucus over the course of both infections. However, plasma cortisol levels were elevated only in the heavily infected fish from the first trial. At high infection levels (Trial 1), alkaline phosphatase activity was higher in the mucus of infected fish at all days (t-test, p < 0.05). However, at the lower infection level (Trial 2), the mucus alkaline phosphatase activity did not differ significantly between infected and non-infected fish. Esterase and lysozyme activities were very low and did not change with time nor between non-infected and infected salmon in either challenge. Mucus enzyme activities of cortisol-implanted salmon did not change over time, nor were there any differences in activities between cortisol-implanted and control salmon. The present study demonstrates biochemical changes resulting from sea lice infection of Atlantic salmon occurring at the site of host-pathogen interaction, the mucus layer. However, the origin of these enzymes, whether host or pathogen, remains to be determined.     

Lessons from sea louse and salmon epidemiology

Effective disease management can benefit from mathematical models that identify drivers of epidemiological change and guide decision-making. This is well illustrated in the host–parasite system of sea lice and salmon, which has been modelled extensively due to the economic costs associated with sea louse infections on salmon farms and the conservation concerns associated with sea louse infections on wild salmon. Consequently, a rich modelling literature devoted to sea louse and salmon epidemiology has been developed. We provide a synthesis of the mathematical and statistical models that have been used to study the epidemiology of sea lice and salmon. These studies span both conceptual and tactical models to quantify the effects of infections on host populations and communities, describe and predict patterns of transmission and dispersal, and guide evidence-based management of wild and farmed salmon. As aquaculture production continues to increase, advances made in modelling sea louse and salmon epidemiology should inform the sustainable management of marine resources.     

Serological evidence of infectious salmon anaemia virus (ISAV) infection in farmed fishes,using an indirect enzyme-linked immunosorbent assay (ELISA)

Antibody detection tests are rarely used for diagnostic purposes in fish diseases. Infectious salmon anaemia (ISA) caused by ISA virus (ISAV) is an emerging disease of Atlantic salmon Salmo salar L. The virus has also been isolated from diseased coho salmon Oncorhynchus kisutch in Chile. An indirect enzyme-linked immunosorbent assay (ELISA) that should facilitate serodiagnosis of ISAV infection, the study of epidemiology, and the control of ISA in farmed fishes has been developed using purified ISAV as the coating antigen, and monoclonal antibodies that detect fish immunoglobulins bound to the antigen on the plate. Application of the test to a random sample of farmed Atlantic salmon from the Bay of Fundy, New Brunswick, Canada, positively identified 5 of the 7 ISAV RT-PCR-positive fish, and all 10 RT-PCR-negative fish were also negative in the ELISA. Some RT-PCR-negative fish had an elevated non-specific antibody reactivity suggestive of chronic infection or resistance to ISAV. This test was also able to detect 11 of the 14 coho salmon pooled serum samples from a clinically affected farm in Chile that were positive by the virus neutralization (VN) test, and 2 of the 4 VN-negative samples. We conclude that this ELISA would be suitable as a routine test for ISAV infection or for assessing ISAV vaccine efficacy before placing smolts in sea cages, and for testing fishes in sea cages to detect level of resistance to ISA. The assay enables vaccination in combination with depopulation control methods.     

Vertical distribution of Atlantic salmon (Salmo salar) as a function of illumination

The vertical distribution of cultured Atlantic salmon larger than 1 kg was monitored by hydroacoustics in both a shallow (6 m) and a deep (20 m) cage. Surface light levels and fish distribution were registered for three periods throughout the year. The two fish groups were fed calculated rations twice a day. During the winter and spring (including vernal equinox), the fish were distributed at around 5 m depth in both cages when not feeding. Around summer solstice, the fish preferred deeper waters when not feeding. The light dependency of the vertical migration was pronounced, and indicates clearly that even a 20 m deep cage is not deep enough to meet the depth requirements of large Atlantic salmon during summer.     

EST and Mitochondrial DNA Sequences Support a Distinct Pacific Form of Salmon Louse, <Emphasis Type="Italic">Lepeophtheirus salmonis</Emphasis>

Nuclear deoxyribonucleic acid sequences from approximately 15,000 salmon louse expressed sequence tags (ESTs), the complete mitochondrial genome (16,148bp) of salmon louse, and 16S ribosomal ribonucleic acid (rRNA) and cytochrome oxidase subunit I (COI) genes from 68 salmon lice collected from Japan, Alaska, and western Canada support a Pacific lineage of Lepeophtheirus salmonis that is distinct from that occurring in the Atlantic Ocean. On average, nuclear genes are 3.2% different, the complete mitochondrial genome is 7.1% different, and 16S rRNA and COI genes are 4.2% and 6.1% different, respectively. Reduced genetic diversity within the Pacific form of L. salmonis is consistent with an introduction into the Pacific from the Atlantic Ocean. The level of divergence is consistent with the hypothesis that the Pacific form of L. salmonis coevolved with Pacific salmon (Onchorhynchus spp.) and the Atlantic form coevolved with Atlantic salmonids (Salmo spp.) independently for the last 2.5–11 million years. The level of genetic divergence coincides with the opportunity for migration of fish between the Atlantic and Pacific Ocean basins via the Arctic Ocean with the opening of the Bering Strait, approximately 5 million years ago. The genetic differences may help explain apparent differences in pathogenicity and environmental sensitivity documented for the Atlantic and Pacific forms of L. salmonis. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.